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e-book Vision and Action: The Control of Grasping

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C Examples of the three main types of neurons recorded during task execution in the light. For each neuron rasters and spike density function are aligned dashed lines on object presentation left part and, after the gap, on the moment when the monkey's hand detached from the starting position right part.

Markers: dark green, cue sound onset beginning of the trial ; light green, end of the cue sound go-signal ; light blue, object pulling onset; orange, end of the trial and reward delivery.

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The task included three basic conditions, as illustrated in Figure 1 B : grasping in the light, grasping in the dark, and a no-go condition. Each of them started when the monkey held its hand on a fixed starting position, after a variable intertrial period ranging from 1 to 1. Grasping in the light : the fixation point was presented and the monkey was required to start fixating it within 1. Fixation onset resulted in the presentation of a cue sound a pure high tone constituted by a Hz sine wave , which instructed the monkey to grasp the subsequently presented object go-cue.

After 0. Then, after a variable time lag 0. It then had to hold the object steadily for at least 0. If the task was performed correctly without breaking fixation, the reward was automatically delivered pressure reward delivery system, Crist Instruments. Grasping in the dark : the entire temporal sequence of events in this condition was identical to that of grasping in the light. However, when the cue sound the same high tone as in grasping in the light ceased go-signal , the light inside the box was automatically switched off and the monkey performed the subsequent motor acts in complete darkness.


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Note that because the fixation point was visible for the entire duration of each trial, it provided a spatial guidance for reaching the object in the absence of visual feedback. No-go condition : the basic sequence of events in this condition was the same as in the other go conditions, but a different cue sound a pure low tone constituted by a Hz sine wave instructed the monkey to remain still and continue fixating the object for 1.

The same sequence of events of the no-go condition has also been employed during a barrier test. In the barrier test, a transparent plastic barrier was interposed between the monkey's hand and the target. The aim of this test was to verify whether object processing by F6 neurons could be different depending on whether the monkey refrained from acting because of a physical obstacle the barrier or because of an instruction cue the no-go signal. Hence, we used the go-cue during this test in order to ensure that the monkey refrained from acting because of the presence of the barrier see also Bonini et al.

Before formal testing of neuronal activity, the monkey was administered a few trials before starting the acquisition block, in order to ensure it actually understood that the barrier was present. The task phases were automatically controlled and monitored by LabView-based software, enabling the interruption of the trial if the monkey broke fixation, made an incorrect movement, or did not respect the task temporal constraints described above. In all these cases, no reward was delivered.

After correct completion of a trial, the monkey was automatically rewarded with the same amount of juice in all conditions. The activity of each neuron was recorded in at least 12 trials for each basic condition. Neurons responding specifically to this condition were not considered as task related in the present study. Reconstruction of the recorded regions and functional maps. Anatomical reconstruction of the right A and left B hemispheres of MK1, with superimposed number and class of neurons recorded from each site. C Anatomical reconstruction of the right hemisphere of MK2, with superimposed number and class of neurons recorded from each site of the 3D probes.

Conventions as in panel B. Note that 2 sites on the most caudal part of the recorded region were associated with face—mouth movement, which is known to correspond to the functional border between areas F3 caudally and F6 rostrally see Luppino et al. The size of the circles corresponds to the current intensity threshold see Materials and Methods. Scale bars in A also applies to B and C. The signal was amplified and sampled at 40 kHz with a channel Omniplex recording system Plexon.

Background

Different sets of 16 channels were recorded only one time during separate sessions on different days. Online spike sorting was performed on all channels using dedicated software Plexon , but all final quantitative analyses were performed off-line, as described in the subsequent sections. Monopolar, biphasic trains of cathodic square wave pulses were delivered through a constant current stimulator PlexStim, Plexon , with the following parameters: total train duration ms, single pulse width 0. At each site, ICMS was delivered when the monkey was quiet and relaxed, and those cases in which monkeys performed voluntary movements were not used to establish the stimulation threshold.

Movements were considered to be evoked by ICMS when 2 experimenters, observing the animal during pulse delivery, independently and repeatedly identified the same joint displacement or muscular twitch, according to previous ICMS studies of the same area Luppino et al. Distinct contact sensitive devices Crist Instruments were used to detect when the monkey grounded touched with the hand the metal surface of the starting position or one of the target objects.

To signal the onset and tonic phase of object pulling, an additional device was connected to the switch located behind each object. Each of these devices provided a TTL signal, which was used by the LabView-based software to monitor the monkey's performance and to control the generation and presentation of the behavioral paradigm's auditory and visual cue signals. Analog signal related to horizontal and vertical eye positions was fed to a computer equipped with dedicated software, enabling calibration and basic processing of eye position signals.

The same software also generated different digital output signals associated with auditory and visual stimuli, the target object presented in each trial, the reward delivery and possible errors made by the monkey during the task i. These signals, together with the TTL signals related to the main behavioral events described above, were fed to the Omniplex system to be recorded together with the neuronal activity and subsequently used to construct the response histograms and the data files for statistical analysis. Single-neuron activity was analyzed in relation to the digital signals related to the main behavioral events, by considering the following epochs of interest: 1 baseline, ms before object presentation; 2 object presentation, from 0 to ms after switching on the light; 3 premovement, ms before reaching onset, signaled by the detachment of monkey's hand from the starting position since an actual movement of the arm does occur to detach the hand from the starting position, this epoch has been considered among those used for the study of motor-related activity ; 4 reaching—grasping, from reaching onset to pulling onset of variable duration, calculated on a trial-by-trial basis ; 5 object holding, from pulling onset to ms after this event.

Note that during baseline, the monkey rested its hand unmovingly on the starting position, was staring at the fixation point, and was already aware of whether the ongoing trial was a go or a no-go trial: these features enabled us to assess possible variation in neural discharge specifically linked with the subsequent task stages within the ongoing behavioral set. Off-line analysis of electromyographic activity of proximal and distal forelimb muscles during task execution has been previously described in both monkeys employed for the present study Bonini et al.

The raw signals were high-pass filtered off-line Hz. Single units were then isolated using principal component and template matching techniques provided by dedicate off-line sorting software Plexon Bonini et al. After identification of well-isolated single units, we classified neurons significantly activated during movement-related epochs relative to baseline, both during grasping in the light and grasping in the dark, separately. Population analyses were carried out taking into account single-neuron responses expressed in terms of normalized mean activity, as previously described elsewhere see Bonini et al.

For each of the recorded neurons, we also calculated the timing of the motor-activity peak. For this purpose, we considered the averaged activity across 12 trials of the same condition in bins of ms, slit forward in steps of 20 ms, within a time window ranging from ms before movement onset to 1 s after this event: the timing associated with the highest among all the obtained values was considered the peak of activity timing. This analysis was performed in ms epochs, slit forward in steps of 20 ms, from ms before to ms after object presentation, and from ms before to ms after movement onset.

The results of this analysis were plotted relative to the center of each epoch by calculating the percentage of significantly tuned neurons in each epoch within each neuronal population see Fig. The histological analysis aimed at identifying the exact location of the implanted probes was performed in both hemispheres of MK1.

The locations of the electrode tracks in the cortex were assessed under an optical microscope in Nissl-stained sections and then plotted and digitized together with the outer and inner borders of the cerebral cortex using a computer-based charting system for the details of the procedure, see Gerbella et al. The cytoarchitectonic features of the recorded region were identified based on the criteria used to subdivide the mesial frontal areas by Matelli et al. Finally, the schematic drawing of the implanted probes was superimposed on the exact location of their traces on oblique re-sliced views of the 3D reconstructions in both hemispheres.

In MK2, which had not yet been sacrificed, the location of the recorded sites was reconstructed based on MRI scan of the monkey's brain performed before the implantation of the head-fixation system and the probes. To obtain a visualization comparable to the one of MK1, MRI slices were directly imported into the aforementioned 3D reconstruction software, together with the stereotaxically measured location of the implanted arrays, in order to obtain the 3D reconstruction as described above.

We recorded a total of single neurons with the task illustrated in Figure 1 B see Bonini et al. Among the task-related neurons, were purely motor, were visuomotor, and 22 were purely visual neurons. Example neurons are shown in Figure 1 C. Neurons classified as purely motor discharged only during reaching—grasping execution Neuron 1.

Visuomotor neurons became active during both the object presentation epoch and reaching—grasping execution Neuron 2 : as exemplified by this neuron, the motor-related discharge of visuomotor neurons was typically characterized by early onset and extremely different dynamics depending on the tested object, often with clearly distinct peaks of visual and motor activity.

Finally, purely visual neurons discharged only during object presentation Neuron 3. Note that all these example neurons also showed differential activation depending on the target object. Table 1 Object preference of all the recorded neurons. Note: a For purely motor neurons, object preference was considered during reaching—grasping execution epochs, whereas for visuomotor and purely visual neurons, object preference was considered during the target presentation epoch.

Neurons were recorded from five chronic arrays constituted by different configurations of linear multielectrode silicon probes see Supplementary Fig. S1 , all implanted in area F6. Figure 2 shows the exact location of the recorded regions in both animals by superimposing a schematic drawing of the implanted probes on 3D reconstructions of the monkey's brain. The recorded regions in both hemispheres of MK1 Fig. The architectonic features of both recorded regions in MK1 indicate that all probes were located within the anatomical borders of area F6 Supplementary Fig.

Because MK2 had not yet been sacrificed, the reconstruction of the recording sites of the 2 probes implanted in its right hemisphere Fig. Figure 2 also shows that visually-triggered neurons i. In particular, we observed complex, multijoint, and relatively slow movements involving the contralateral arm and the shoulder, often including the wrist and the hand dark green circles in Fig. Among purely motor neurons, 32 Figure 3 A shows examples of grip-selective F6 motor neurons tested during reaching—grasping in the light and in the dark.

Neuron 1 is a typical example of a grip-selective neuron, which discharged more strongly when the monkey grasped the ring regardless of whether grasping was performed in the light or in the dark. Neuron 2 exhibited a preferential discharge for the big cone, but its activity was stronger during grasping in the light, whereas Neuron 3 showed the opposite modulation, being more strongly activated during grasping in the dark than in the light, with a preferential discharge for the big and small cones relative to the ring.

It is clear from the neuron examples that the target selectivity of F6 purely motor neurons cannot be accounted for by vision of the object. This conclusion is also supported by population activity, which shows that both motor activity and object selectivity assessed during grasping in the light remained the same even during grasping in the dark Fig. Functional properties of F6 purely motor neurons. A Examples of three F6 purely motor neurons showing selectivity for the target object. The image on the left of each line of the panel shows the type of grip employed by the monkey in that trials.

Other conventions and markers as in Figure 1. B Population activity of purely motor neurons with object selectivity. As for single-neuron examples, the activity is aligned to the movement onset, and shows the averaged population response to the preferred and non-preferred target established on the basis of each neurons response during grasping in the light.

The Control of Grasping

The colored shaded area around each curve represents 1 standard error. C Number of purely motor neurons with selectivity for 1 or 2 of the target objects, or with no object selectivity. Functional properties of F6 visually-triggered neurons. A Examples of three F6 visually-triggered neurons showing visual selectivity for the target object.


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  6. For each neuron, rasters and spike density function have been aligned dashed lines to three different events, separated by a gap: 1 object presentation during no-go trials on the left ; 2 object presentation during go trials on the center ; 3 movement onset on the right. Red triangular marker, no-go cue sound onset beginning of the trial. Other conventions as in Figure 1. B Population activity of visually-triggered neurons with object selectivity. Best red and worst gray objects have been selected, for each neuron, based on the visual response during go-trials.

    In the no-go condition, the activity is aligned to the object presentation dashed line on the left and, after the gap, to the no-go signal dashed line on the right. In the go condition, the activity is aligned to the object presentation dashed line on the left and, after the gap, to the movement onset dashed line on the right. C Number of visually-triggered neurons with visual selectivity for 1 or 2 of the target objects, or with no object selectivity.

    Another important finding is that object visual selectivity displayed by F6 neuronal population during go trials was also present during no-go trials, even though the discharge intensity was significantly reduced. This suggests that visually-triggered F6 neurons underlie visuomotor associations between observed objects and the potential motor actions that can be performed on them. An interesting observation supporting this hypothesis is that visually-triggered neurons exhibited a preferential selectivity for the ring, in contrast to the balanced motor selectivity for the different objects of purely motor neurons see above , which rules out possible interpretations of this findings in terms of a sampling bias.

    This finding may be due to the well-established role of F6 in forming new arbitrarily learned visuomotor associations Nakamura et al. This latter grip type was achieved through a specific training, which may explain its visual overrepresentation. Visual responses of F6 neurons to object presentation in different contexts.

    A Example of an F6 visually-triggered neuron showing visual selectivity for the small and the big cone and reduced response and selectivity when tested with a plastic barrier interposed between monkey's hand and the target. Conventions as in Figure 1. B Population activity of all F6 visually-triggered neurons tested in the three conditions. The population response to the presentation of the worst object did not differ significantly among any of the compared conditions go vs.

    According to a widely accepted view, the mesial premotor cortex encodes triggering signals for starting and sequencing self-initiated actions, whose details, such as reach direction and grip type, are processed by dorsolateral premotor areas by means of parieto-premotor interactions Rizzolatti and Luppino ; Cisek and Kalaska ; Kaas and Stepniewska In order to investigate the relative contribution of mesial and ventral premotor areas in reaching—grasping actions, we compared the response properties of neurons recorded from area F6 in this study with those previously recorded from area F5 with the same behavioral paradigm and in the same animals see Bonini et al.

    Comparison of neuronal dynamic and object selectivity between F5 and F6 visuomotor and purely motor neurons. Normalized activity of A visuomotor and C purely motor neurons of area F6 ordered based on the timing of their peak of motor activity earliest on bottom. Each row represents a single neuron.

    White dashed lines represent the different alignment events: first on the left, before the gap object presentation, second on the right, after the gap hand movement onset. Black dashed lines correspond to the same alignment events described in A and C. Other conventions as in Figure 4 B. E — H Normalized single neuron E and G and population F and H activity of visuomotor and purely motor neurons recorded from area F5 of the same animals and with the same task.

    All conventions as in A — D. Comparison of object visual and motor selectivity of F5 and F6 neurons. According to several neurophysiological studies, the pre-supplementary motor cortex plays a crucial role in complex sequential and cognitive processes underlying simple movements required as a response in a behavioral task Tanji ; Akkal et al. The same type of task of the present study has been typically used to investigate the properties of neurons in other areas of the cortical grasping network.

    Indeed, our findings indicate that a subset of F6 neurons can exhibit object-selective visual and motor responses. Most interestingly, visuomotor and purely motor F6 neurons appear to form 2 functionally distinct populations, in striking contrast to the dynamic visual-to-motor processing displayed by F5 visuomotor single-neuron and population activity. Furthermore, the visual processing of objects by area F6 neurons appears to be context-dependent, because neuronal selectivity was stronger when target presentation occurred in the context of go trials relative to no-go trials, and was completely abolished when, in spite of the instruction to go, a transparent barrier was interposed between the monkey's hand and the target, preventing the animal from reaching it.

    Altogether, these findings suggest that F6 visual activity can provide a motor representation of the impending object-directed action, which is conditional upon both the monkey's intention and possibility to perform it. One of the most striking findings in the anatomical literature concerning area F6 is that, as compared with the adjacent supplementary motor area F3, it completely lacks direct connections with the spinal cord and the primary motor cortex He et al.

    Hence, its contribution to grasping actions has to be mediated by other anatomically connected areas. Anatomical connections with area F6 have in fact been demonstrated for all the main premotor Matelli et al. Furthermore, F6 is consistently linked with the prefrontal cortex, particularly with the intermediate part of the convexity and bank portions of both dorsal Saleem et al.

    Interestingly, in this latter sector, neurons related to reaching—grasping actions have been recently described Simone et al. Finally, area F6 is also heavily connected with sectors of the basal ganglia Parthasarathy et al. In summary, anatomical data support the possibility that F6 plays a role in reaching—grasping actions by integrating a wide range of information and influencing, both directly and indirectly, the processing operations carried out by the core areas of the grasping network.

    First, we showed that neuronal discharge and object selectivity of F6 purely motor neurons were the same during grasping in both the light and the dark, indicating that their activity truly reflects a motor encoding of the hand grip, as previously shown for F5 Raos et al.

    Second, both the visual presentation response and object selectivity of F6 visuomotor neurons were stronger during go trials, which is consistent with previous findings in F5 Raos et al. Third, the barrier test revealed that object selectivity was abolished when a transparent barrier was interposed between the monkey's hand and the target, as demonstrated for area F5 visuomotor neurons see Bonini et al. In spite of the functional analogies so far described and the tight reciprocal anatomical connections between F6 and F5 that could account for them, it is unlikely that these 2 areas provide a similar contribution to grasping actions.

    For example, it has been directly demonstrated that the inactivation of area F5 in monkeys impairs visually guided grasping of objects, providing causal evidence that this region plays a crucial role in controlling the hand shape for appropriately interacting with the target Fogassi et al. In contrast, reaching—grasping actions are virtually unimpaired following large lesions of the pre-supplementary motor cortex Brinkman and Porter ; Thaler et al.

    These findings would suggest that normal manual behavior is the result of a control exerted by mesial premotor areas on the lateral premotor cortex. Our data reveal that area F6 can play a role in the visuomotor representation of objects and of how they can be grasped, and provide the opportunity for a direct comparison with the functional properties of area F5 neurons.

    Convergent evidence from several studies indicates the existence of a typical visual-to-motor response pattern in all the parietal Sakata et al. Based on the fundamental differences we found between the single neuron and population activity of F6 and F5, it appears to be unlikely that F6 neurons play a role in visuomotor transformation. Instead, an interesting and more plausible interpretation can be suggested by considering the specific aspects of the neuronal visuomotor processing that characterize the 2 areas.

    From vision to hand action: Neuroscientists decipher how our brain controls grasping movements

    Our findings show that area F6 single neurons peak relatively earlier and display shorter bursts of phasic activity relative to those of F5 Fig. At the population level, these differences translate into even more clear-cut evidence: though being anatomically intermingled, like those of F5 Bonini et al. The former provides mainly a visual processing of the object Fig. In line with this difference, we also found a set of F6 neurons with purely visual response properties see Table 1 , which are virtually absent in area F5. Interestingly, area F6 purely visual neurons can also display contextual selectivity for go or no-go trials see the example Neuron 1 in Fig.

    More importantly, we observed a clear difference in the tuning for specific objects between the 2 areas. Indeed, F6 exhibited a bias in its visual and preparatory activity for the ring i. This finding suggests that in F6 the processing of overlearned visuomotor associations prevails, whereas in F5 there is a preferential coding of the visuomotor transformations related to the grip types belonging to the monkey's natural behavioral repertoire Macfarlane and Graziano How could visuomotor transformation and association processes interact?

    Typically, the same object can offer multiple grip affordances. Among them, we select the most appropriate depending on the current contextual situation, the goal we are pursuing, or specific instructions. Interestingly, Fluet et al.

    Frontiers | Thirst for Intention? Grasping a Glass Is a Thirst-Controlled Action | Psychology

    Furthermore, using a similar paradigm, Vargas-Irwin et al. Therefore, it is clear that in area F5, the visuomotor transformation of an object's visual features into the motor plans required for grasping it are flexibly modulated by learned visuomotor associations.

    The aim of this test was to verify whether object processing by F6 neurons could be different depending on whether the monkey refrained from acting because of a physical obstacle the barrier or because of an instruction cue the no-go signal. Hence, we used the go-cue during this test in order to ensure that the monkey refrained from acting because of the presence of the barrier see also Bonini et al.

    Before formal testing of neuronal activity, the monkey was administered a few trials before starting the acquisition block, in order to ensure it actually understood that the barrier was present. The task phases were automatically controlled and monitored by LabView-based software, enabling the interruption of the trial if the monkey broke fixation, made an incorrect movement, or did not respect the task temporal constraints described above. In all these cases, no reward was delivered. After correct completion of a trial, the monkey was automatically rewarded with the same amount of juice in all conditions.

    The activity of each neuron was recorded in at least 12 trials for each basic condition. Neurons responding specifically to this condition were not considered as task related in the present study. Reconstruction of the recorded regions and functional maps. Anatomical reconstruction of the right A and left B hemispheres of MK1, with superimposed number and class of neurons recorded from each site.

    C Anatomical reconstruction of the right hemisphere of MK2, with superimposed number and class of neurons recorded from each site of the 3D probes. Conventions as in panel B. Note that 2 sites on the most caudal part of the recorded region were associated with face—mouth movement, which is known to correspond to the functional border between areas F3 caudally and F6 rostrally see Luppino et al.

    The size of the circles corresponds to the current intensity threshold see Materials and Methods. Scale bars in A also applies to B and C. The signal was amplified and sampled at 40 kHz with a channel Omniplex recording system Plexon. Different sets of 16 channels were recorded only one time during separate sessions on different days.

    Online spike sorting was performed on all channels using dedicated software Plexon , but all final quantitative analyses were performed off-line, as described in the subsequent sections.

    Video-based Prediction of Hand-grasp Preshaping with Application to Prosthesis Control

    Monopolar, biphasic trains of cathodic square wave pulses were delivered through a constant current stimulator PlexStim, Plexon , with the following parameters: total train duration ms, single pulse width 0. At each site, ICMS was delivered when the monkey was quiet and relaxed, and those cases in which monkeys performed voluntary movements were not used to establish the stimulation threshold. Movements were considered to be evoked by ICMS when 2 experimenters, observing the animal during pulse delivery, independently and repeatedly identified the same joint displacement or muscular twitch, according to previous ICMS studies of the same area Luppino et al.

    Distinct contact sensitive devices Crist Instruments were used to detect when the monkey grounded touched with the hand the metal surface of the starting position or one of the target objects. To signal the onset and tonic phase of object pulling, an additional device was connected to the switch located behind each object.

    Each of these devices provided a TTL signal, which was used by the LabView-based software to monitor the monkey's performance and to control the generation and presentation of the behavioral paradigm's auditory and visual cue signals. Analog signal related to horizontal and vertical eye positions was fed to a computer equipped with dedicated software, enabling calibration and basic processing of eye position signals.

    The same software also generated different digital output signals associated with auditory and visual stimuli, the target object presented in each trial, the reward delivery and possible errors made by the monkey during the task i. These signals, together with the TTL signals related to the main behavioral events described above, were fed to the Omniplex system to be recorded together with the neuronal activity and subsequently used to construct the response histograms and the data files for statistical analysis.

    Single-neuron activity was analyzed in relation to the digital signals related to the main behavioral events, by considering the following epochs of interest: 1 baseline, ms before object presentation; 2 object presentation, from 0 to ms after switching on the light; 3 premovement, ms before reaching onset, signaled by the detachment of monkey's hand from the starting position since an actual movement of the arm does occur to detach the hand from the starting position, this epoch has been considered among those used for the study of motor-related activity ; 4 reaching—grasping, from reaching onset to pulling onset of variable duration, calculated on a trial-by-trial basis ; 5 object holding, from pulling onset to ms after this event.

    Note that during baseline, the monkey rested its hand unmovingly on the starting position, was staring at the fixation point, and was already aware of whether the ongoing trial was a go or a no-go trial: these features enabled us to assess possible variation in neural discharge specifically linked with the subsequent task stages within the ongoing behavioral set.

    Off-line analysis of electromyographic activity of proximal and distal forelimb muscles during task execution has been previously described in both monkeys employed for the present study Bonini et al. The raw signals were high-pass filtered off-line Hz. Single units were then isolated using principal component and template matching techniques provided by dedicate off-line sorting software Plexon Bonini et al.

    After identification of well-isolated single units, we classified neurons significantly activated during movement-related epochs relative to baseline, both during grasping in the light and grasping in the dark, separately. Population analyses were carried out taking into account single-neuron responses expressed in terms of normalized mean activity, as previously described elsewhere see Bonini et al.

    For each of the recorded neurons, we also calculated the timing of the motor-activity peak. For this purpose, we considered the averaged activity across 12 trials of the same condition in bins of ms, slit forward in steps of 20 ms, within a time window ranging from ms before movement onset to 1 s after this event: the timing associated with the highest among all the obtained values was considered the peak of activity timing. This analysis was performed in ms epochs, slit forward in steps of 20 ms, from ms before to ms after object presentation, and from ms before to ms after movement onset.

    The results of this analysis were plotted relative to the center of each epoch by calculating the percentage of significantly tuned neurons in each epoch within each neuronal population see Fig. The histological analysis aimed at identifying the exact location of the implanted probes was performed in both hemispheres of MK1. The locations of the electrode tracks in the cortex were assessed under an optical microscope in Nissl-stained sections and then plotted and digitized together with the outer and inner borders of the cerebral cortex using a computer-based charting system for the details of the procedure, see Gerbella et al.

    The cytoarchitectonic features of the recorded region were identified based on the criteria used to subdivide the mesial frontal areas by Matelli et al. Finally, the schematic drawing of the implanted probes was superimposed on the exact location of their traces on oblique re-sliced views of the 3D reconstructions in both hemispheres.

    In MK2, which had not yet been sacrificed, the location of the recorded sites was reconstructed based on MRI scan of the monkey's brain performed before the implantation of the head-fixation system and the probes. To obtain a visualization comparable to the one of MK1, MRI slices were directly imported into the aforementioned 3D reconstruction software, together with the stereotaxically measured location of the implanted arrays, in order to obtain the 3D reconstruction as described above.

    We recorded a total of single neurons with the task illustrated in Figure 1 B see Bonini et al. Among the task-related neurons, were purely motor, were visuomotor, and 22 were purely visual neurons. Example neurons are shown in Figure 1 C. Neurons classified as purely motor discharged only during reaching—grasping execution Neuron 1. Visuomotor neurons became active during both the object presentation epoch and reaching—grasping execution Neuron 2 : as exemplified by this neuron, the motor-related discharge of visuomotor neurons was typically characterized by early onset and extremely different dynamics depending on the tested object, often with clearly distinct peaks of visual and motor activity.

    Finally, purely visual neurons discharged only during object presentation Neuron 3. Note that all these example neurons also showed differential activation depending on the target object. Table 1 Object preference of all the recorded neurons.

    Background

    Note: a For purely motor neurons, object preference was considered during reaching—grasping execution epochs, whereas for visuomotor and purely visual neurons, object preference was considered during the target presentation epoch. Neurons were recorded from five chronic arrays constituted by different configurations of linear multielectrode silicon probes see Supplementary Fig.

    S1 , all implanted in area F6. Figure 2 shows the exact location of the recorded regions in both animals by superimposing a schematic drawing of the implanted probes on 3D reconstructions of the monkey's brain. The recorded regions in both hemispheres of MK1 Fig. The architectonic features of both recorded regions in MK1 indicate that all probes were located within the anatomical borders of area F6 Supplementary Fig. Because MK2 had not yet been sacrificed, the reconstruction of the recording sites of the 2 probes implanted in its right hemisphere Fig.

    Figure 2 also shows that visually-triggered neurons i. In particular, we observed complex, multijoint, and relatively slow movements involving the contralateral arm and the shoulder, often including the wrist and the hand dark green circles in Fig. Among purely motor neurons, 32 Figure 3 A shows examples of grip-selective F6 motor neurons tested during reaching—grasping in the light and in the dark. Neuron 1 is a typical example of a grip-selective neuron, which discharged more strongly when the monkey grasped the ring regardless of whether grasping was performed in the light or in the dark.

    Neuron 2 exhibited a preferential discharge for the big cone, but its activity was stronger during grasping in the light, whereas Neuron 3 showed the opposite modulation, being more strongly activated during grasping in the dark than in the light, with a preferential discharge for the big and small cones relative to the ring. It is clear from the neuron examples that the target selectivity of F6 purely motor neurons cannot be accounted for by vision of the object.

    This conclusion is also supported by population activity, which shows that both motor activity and object selectivity assessed during grasping in the light remained the same even during grasping in the dark Fig. Functional properties of F6 purely motor neurons. A Examples of three F6 purely motor neurons showing selectivity for the target object. The image on the left of each line of the panel shows the type of grip employed by the monkey in that trials.

    Other conventions and markers as in Figure 1. B Population activity of purely motor neurons with object selectivity. As for single-neuron examples, the activity is aligned to the movement onset, and shows the averaged population response to the preferred and non-preferred target established on the basis of each neurons response during grasping in the light.

    The colored shaded area around each curve represents 1 standard error. C Number of purely motor neurons with selectivity for 1 or 2 of the target objects, or with no object selectivity. Functional properties of F6 visually-triggered neurons. A Examples of three F6 visually-triggered neurons showing visual selectivity for the target object. For each neuron, rasters and spike density function have been aligned dashed lines to three different events, separated by a gap: 1 object presentation during no-go trials on the left ; 2 object presentation during go trials on the center ; 3 movement onset on the right.

    Red triangular marker, no-go cue sound onset beginning of the trial. Other conventions as in Figure 1. B Population activity of visually-triggered neurons with object selectivity. Best red and worst gray objects have been selected, for each neuron, based on the visual response during go-trials. In the no-go condition, the activity is aligned to the object presentation dashed line on the left and, after the gap, to the no-go signal dashed line on the right. In the go condition, the activity is aligned to the object presentation dashed line on the left and, after the gap, to the movement onset dashed line on the right.

    C Number of visually-triggered neurons with visual selectivity for 1 or 2 of the target objects, or with no object selectivity. Another important finding is that object visual selectivity displayed by F6 neuronal population during go trials was also present during no-go trials, even though the discharge intensity was significantly reduced. This suggests that visually-triggered F6 neurons underlie visuomotor associations between observed objects and the potential motor actions that can be performed on them.

    An interesting observation supporting this hypothesis is that visually-triggered neurons exhibited a preferential selectivity for the ring, in contrast to the balanced motor selectivity for the different objects of purely motor neurons see above , which rules out possible interpretations of this findings in terms of a sampling bias.

    This finding may be due to the well-established role of F6 in forming new arbitrarily learned visuomotor associations Nakamura et al. This latter grip type was achieved through a specific training, which may explain its visual overrepresentation. Visual responses of F6 neurons to object presentation in different contexts. A Example of an F6 visually-triggered neuron showing visual selectivity for the small and the big cone and reduced response and selectivity when tested with a plastic barrier interposed between monkey's hand and the target. Conventions as in Figure 1.

    B Population activity of all F6 visually-triggered neurons tested in the three conditions. The population response to the presentation of the worst object did not differ significantly among any of the compared conditions go vs. According to a widely accepted view, the mesial premotor cortex encodes triggering signals for starting and sequencing self-initiated actions, whose details, such as reach direction and grip type, are processed by dorsolateral premotor areas by means of parieto-premotor interactions Rizzolatti and Luppino ; Cisek and Kalaska ; Kaas and Stepniewska In order to investigate the relative contribution of mesial and ventral premotor areas in reaching—grasping actions, we compared the response properties of neurons recorded from area F6 in this study with those previously recorded from area F5 with the same behavioral paradigm and in the same animals see Bonini et al.

    Comparison of neuronal dynamic and object selectivity between F5 and F6 visuomotor and purely motor neurons. Normalized activity of A visuomotor and C purely motor neurons of area F6 ordered based on the timing of their peak of motor activity earliest on bottom. Each row represents a single neuron. White dashed lines represent the different alignment events: first on the left, before the gap object presentation, second on the right, after the gap hand movement onset.

    Black dashed lines correspond to the same alignment events described in A and C. Other conventions as in Figure 4 B. E — H Normalized single neuron E and G and population F and H activity of visuomotor and purely motor neurons recorded from area F5 of the same animals and with the same task. All conventions as in A — D. Comparison of object visual and motor selectivity of F5 and F6 neurons. According to several neurophysiological studies, the pre-supplementary motor cortex plays a crucial role in complex sequential and cognitive processes underlying simple movements required as a response in a behavioral task Tanji ; Akkal et al.

    The same type of task of the present study has been typically used to investigate the properties of neurons in other areas of the cortical grasping network. Indeed, our findings indicate that a subset of F6 neurons can exhibit object-selective visual and motor responses. Most interestingly, visuomotor and purely motor F6 neurons appear to form 2 functionally distinct populations, in striking contrast to the dynamic visual-to-motor processing displayed by F5 visuomotor single-neuron and population activity.

    Furthermore, the visual processing of objects by area F6 neurons appears to be context-dependent, because neuronal selectivity was stronger when target presentation occurred in the context of go trials relative to no-go trials, and was completely abolished when, in spite of the instruction to go, a transparent barrier was interposed between the monkey's hand and the target, preventing the animal from reaching it. Altogether, these findings suggest that F6 visual activity can provide a motor representation of the impending object-directed action, which is conditional upon both the monkey's intention and possibility to perform it.

    One of the most striking findings in the anatomical literature concerning area F6 is that, as compared with the adjacent supplementary motor area F3, it completely lacks direct connections with the spinal cord and the primary motor cortex He et al. Hence, its contribution to grasping actions has to be mediated by other anatomically connected areas. Anatomical connections with area F6 have in fact been demonstrated for all the main premotor Matelli et al. Furthermore, F6 is consistently linked with the prefrontal cortex, particularly with the intermediate part of the convexity and bank portions of both dorsal Saleem et al.

    Interestingly, in this latter sector, neurons related to reaching—grasping actions have been recently described Simone et al. Finally, area F6 is also heavily connected with sectors of the basal ganglia Parthasarathy et al.

    In summary, anatomical data support the possibility that F6 plays a role in reaching—grasping actions by integrating a wide range of information and influencing, both directly and indirectly, the processing operations carried out by the core areas of the grasping network.

    First, we showed that neuronal discharge and object selectivity of F6 purely motor neurons were the same during grasping in both the light and the dark, indicating that their activity truly reflects a motor encoding of the hand grip, as previously shown for F5 Raos et al. Second, both the visual presentation response and object selectivity of F6 visuomotor neurons were stronger during go trials, which is consistent with previous findings in F5 Raos et al.

    Third, the barrier test revealed that object selectivity was abolished when a transparent barrier was interposed between the monkey's hand and the target, as demonstrated for area F5 visuomotor neurons see Bonini et al. In spite of the functional analogies so far described and the tight reciprocal anatomical connections between F6 and F5 that could account for them, it is unlikely that these 2 areas provide a similar contribution to grasping actions. For example, it has been directly demonstrated that the inactivation of area F5 in monkeys impairs visually guided grasping of objects, providing causal evidence that this region plays a crucial role in controlling the hand shape for appropriately interacting with the target Fogassi et al.

    In contrast, reaching—grasping actions are virtually unimpaired following large lesions of the pre-supplementary motor cortex Brinkman and Porter ; Thaler et al. These findings would suggest that normal manual behavior is the result of a control exerted by mesial premotor areas on the lateral premotor cortex. Our data reveal that area F6 can play a role in the visuomotor representation of objects and of how they can be grasped, and provide the opportunity for a direct comparison with the functional properties of area F5 neurons.

    Convergent evidence from several studies indicates the existence of a typical visual-to-motor response pattern in all the parietal Sakata et al. Based on the fundamental differences we found between the single neuron and population activity of F6 and F5, it appears to be unlikely that F6 neurons play a role in visuomotor transformation.

    Instead, an interesting and more plausible interpretation can be suggested by considering the specific aspects of the neuronal visuomotor processing that characterize the 2 areas. Our findings show that area F6 single neurons peak relatively earlier and display shorter bursts of phasic activity relative to those of F5 Fig. At the population level, these differences translate into even more clear-cut evidence: though being anatomically intermingled, like those of F5 Bonini et al.

    The former provides mainly a visual processing of the object Fig. In line with this difference, we also found a set of F6 neurons with purely visual response properties see Table 1 , which are virtually absent in area F5. Interestingly, area F6 purely visual neurons can also display contextual selectivity for go or no-go trials see the example Neuron 1 in Fig. More importantly, we observed a clear difference in the tuning for specific objects between the 2 areas.

    Indeed, F6 exhibited a bias in its visual and preparatory activity for the ring i. This finding suggests that in F6 the processing of overlearned visuomotor associations prevails, whereas in F5 there is a preferential coding of the visuomotor transformations related to the grip types belonging to the monkey's natural behavioral repertoire Macfarlane and Graziano How could visuomotor transformation and association processes interact?

    Typically, the same object can offer multiple grip affordances. Among them, we select the most appropriate depending on the current contextual situation, the goal we are pursuing, or specific instructions.

    Interestingly, Fluet et al. Furthermore, using a similar paradigm, Vargas-Irwin et al. Therefore, it is clear that in area F5, the visuomotor transformation of an object's visual features into the motor plans required for grasping it are flexibly modulated by learned visuomotor associations. The present findings suggest that F6 may encode visuomotor associations between specific elements of contextual information, likely conveyed by the prefrontal cortex, and motor representations of reaching—grasping actions.

    Although a similar role might be hypothesized for other ventral frontal regions connected with F6, such as the so-called pre-PMv Dancause et al. The present findings are in line with previous proposals Rizzolatti and Luppino maintaining that area F6 constitutes a prefronto-dependent area that forms a bridge between highly cognitive, context-based neuronal operations, on one side, and the parieto-dependent visuomotor transformations underlying the flow of voluntary actions, on the other.

    However, our findings also suggest to extend the existing models of the organization of reaching—grasping intentional actions Fagg and Arbib by including the pre-supplementary motor area as a relevant, additional node of the cortical grasping network that plays a role in the integration of visuomotor transformation and sensorimotor association processes for action organization. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide.

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