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Dynamic social adaptation of motion-related neurons in primate parietal cortex.

Fujii N, Hihara S, Iriki A - PLoS ONE (2007)

Bottom Line: Under these circumstances, parietal neurons started to show complex combinatorial responses to motion of self and other.Parietal cortex adapted its response properties in the social context by discarding and recruiting different neural populations.Our results suggest that parietal neurons can recognize social events in the environment linked with current social context and form part of a larger social brain network.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Symbolic Cognitive Development, RIKEN Brain Science Institute, Wako, Japan. na@brain.riken.jp

ABSTRACT
Social brain function, which allows us to adapt our behavior to social context, is poorly understood at the single-cell level due largely to technical limitations. But the questions involved are vital: How do neurons recognize and modulate their activity in response to social context? To probe the mechanisms involved, we developed a novel recording technique, called multi-dimensional recording, and applied it simultaneously in the left parietal cortices of two monkeys while they shared a common social space. When the monkeys sat near each other but did not interact, each monkey's parietal activity showed robust response preference to action by his own right arm and almost no response to action by the other's arm. But the preference was broken if social conflict emerged between the monkeys-specifically, if both were able to reach for the same food item placed on the table between them. Under these circumstances, parietal neurons started to show complex combinatorial responses to motion of self and other. Parietal cortex adapted its response properties in the social context by discarding and recruiting different neural populations. Our results suggest that parietal neurons can recognize social events in the environment linked with current social context and form part of a larger social brain network.

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Schematic top views of the task environment for positions A–C, and recording map.During these tasks, we put two monkeys in one of three relative positions (A, B and C) around a table. Each monkey is identified by the color of the circle on his head (green, M1; red, M2). On each trial, we placed a food item at one of four locations in position A and one of three locations in position B and C, indicated by circles on the table. Each circle on the table is a pie chart that depicts each monkey's success ratio for food retrieval in that table location. D. Recording tracks are indicated by blue dots on the brain. The size of each circle centered on the track indicates the number of MR neurons recorded from the track. Green dots indicate the locations of lesion markers for reconstruction.
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pone-0000397-g001: Schematic top views of the task environment for positions A–C, and recording map.During these tasks, we put two monkeys in one of three relative positions (A, B and C) around a table. Each monkey is identified by the color of the circle on his head (green, M1; red, M2). On each trial, we placed a food item at one of four locations in position A and one of three locations in position B and C, indicated by circles on the table. Each circle on the table is a pie chart that depicts each monkey's success ratio for food retrieval in that table location. D. Recording tracks are indicated by blue dots on the brain. The size of each circle centered on the track indicates the number of MR neurons recorded from the track. Green dots indicate the locations of lesion markers for reconstruction.

Mentions: Two male Japanese macaque monkeys (Macaca fuscata), here called M1 and M2, were used. All procedures were approved in advance by the RIKEN Animal Committee (H18-2B012). A recording chamber was surgically implanted in the left hemisphere of each monkey. We chronically implanted twelve tungsten electrodes (FHC: impedance 800 K–1 M ohm), aiming to record neural activity in an area anterior to the intra-parietal sulcus (IPS) [6]. Most of the motion-related neurons from which we recorded were located in the anterior/medial wall of the IPS (Figure 1D), and were identified by MRI images taken before the experiment. Neuronal activity was recorded by the Digital Lynx system (Neuralynx, Tucson, AZ) and subsequently sorted individually by manual parameters with the Offline Sorter (Plexon, Dallas, TX). Before starting neural recording, we tested the neurons' somatosensory responses. Most of them showed somatosensory responses to right, but occasionally on left, palm, distal and proximal arm, and shoulder. We monitored arm and head movements with a Vicon motion capture system (Vicon Peak, Oxford, UK), sampling at 120 Hz. Monkeys wore motion capture suits which were custom ordered for each monkey. Ten reflective markers (bilateral shoulder, elbow, wrist and hand, as well as forehead and back of head) were attached to each motion capture suit and their locations were reconstructed in three dimensions by the motion capture system. Eight video cameras recorded the entire experimental environment. At the beginning of each recording session we adjusted each electrode's position to obtain the best signal-to-noise ratio, but did not reposition the electrodes during the sessions. During each recording session, neuronal activity was stable and the monkeys' free behavior did not contaminate the neural data with artifact noise. Neural data were collected from nine recording sessions.


Dynamic social adaptation of motion-related neurons in primate parietal cortex.

Fujii N, Hihara S, Iriki A - PLoS ONE (2007)

Schematic top views of the task environment for positions A–C, and recording map.During these tasks, we put two monkeys in one of three relative positions (A, B and C) around a table. Each monkey is identified by the color of the circle on his head (green, M1; red, M2). On each trial, we placed a food item at one of four locations in position A and one of three locations in position B and C, indicated by circles on the table. Each circle on the table is a pie chart that depicts each monkey's success ratio for food retrieval in that table location. D. Recording tracks are indicated by blue dots on the brain. The size of each circle centered on the track indicates the number of MR neurons recorded from the track. Green dots indicate the locations of lesion markers for reconstruction.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC1851098&req=5

pone-0000397-g001: Schematic top views of the task environment for positions A–C, and recording map.During these tasks, we put two monkeys in one of three relative positions (A, B and C) around a table. Each monkey is identified by the color of the circle on his head (green, M1; red, M2). On each trial, we placed a food item at one of four locations in position A and one of three locations in position B and C, indicated by circles on the table. Each circle on the table is a pie chart that depicts each monkey's success ratio for food retrieval in that table location. D. Recording tracks are indicated by blue dots on the brain. The size of each circle centered on the track indicates the number of MR neurons recorded from the track. Green dots indicate the locations of lesion markers for reconstruction.
Mentions: Two male Japanese macaque monkeys (Macaca fuscata), here called M1 and M2, were used. All procedures were approved in advance by the RIKEN Animal Committee (H18-2B012). A recording chamber was surgically implanted in the left hemisphere of each monkey. We chronically implanted twelve tungsten electrodes (FHC: impedance 800 K–1 M ohm), aiming to record neural activity in an area anterior to the intra-parietal sulcus (IPS) [6]. Most of the motion-related neurons from which we recorded were located in the anterior/medial wall of the IPS (Figure 1D), and were identified by MRI images taken before the experiment. Neuronal activity was recorded by the Digital Lynx system (Neuralynx, Tucson, AZ) and subsequently sorted individually by manual parameters with the Offline Sorter (Plexon, Dallas, TX). Before starting neural recording, we tested the neurons' somatosensory responses. Most of them showed somatosensory responses to right, but occasionally on left, palm, distal and proximal arm, and shoulder. We monitored arm and head movements with a Vicon motion capture system (Vicon Peak, Oxford, UK), sampling at 120 Hz. Monkeys wore motion capture suits which were custom ordered for each monkey. Ten reflective markers (bilateral shoulder, elbow, wrist and hand, as well as forehead and back of head) were attached to each motion capture suit and their locations were reconstructed in three dimensions by the motion capture system. Eight video cameras recorded the entire experimental environment. At the beginning of each recording session we adjusted each electrode's position to obtain the best signal-to-noise ratio, but did not reposition the electrodes during the sessions. During each recording session, neuronal activity was stable and the monkeys' free behavior did not contaminate the neural data with artifact noise. Neural data were collected from nine recording sessions.

Bottom Line: Under these circumstances, parietal neurons started to show complex combinatorial responses to motion of self and other.Parietal cortex adapted its response properties in the social context by discarding and recruiting different neural populations.Our results suggest that parietal neurons can recognize social events in the environment linked with current social context and form part of a larger social brain network.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Symbolic Cognitive Development, RIKEN Brain Science Institute, Wako, Japan. na@brain.riken.jp

ABSTRACT
Social brain function, which allows us to adapt our behavior to social context, is poorly understood at the single-cell level due largely to technical limitations. But the questions involved are vital: How do neurons recognize and modulate their activity in response to social context? To probe the mechanisms involved, we developed a novel recording technique, called multi-dimensional recording, and applied it simultaneously in the left parietal cortices of two monkeys while they shared a common social space. When the monkeys sat near each other but did not interact, each monkey's parietal activity showed robust response preference to action by his own right arm and almost no response to action by the other's arm. But the preference was broken if social conflict emerged between the monkeys-specifically, if both were able to reach for the same food item placed on the table between them. Under these circumstances, parietal neurons started to show complex combinatorial responses to motion of self and other. Parietal cortex adapted its response properties in the social context by discarding and recruiting different neural populations. Our results suggest that parietal neurons can recognize social events in the environment linked with current social context and form part of a larger social brain network.

Show MeSH