Somato-Motor Haptic Processing in Posterior Inner Perisylvian Region (SII/pIC) of the Macaque Monkey

Abstract

The posterior inner perisylvian region including the secondary somatosensory cortex (area SII) and the adjacent region of posterior insular cortex (pIC) has been implicated in haptic processing by integrating somato-motor information during hand-manipulation, both in humans and in non-human primates. However, motor-related properties during hand-manipulation are still largely unknown. To investigate a motor-related activity in the hand region of SII/pIC, two macaque monkeys were trained to perform a hand-manipulation task, requiring 3 different grip types (precision grip, finger exploration, side grip) both in light and in dark conditions. Our results showed that 70% (n = 33/48) of task related neurons within SII/pIC were only activated during monkeys’ active hand-manipulation. Of those 33 neurons, 15 (45%) began to discharge before hand-target contact, while the remaining neurons were tonically active after contact. Thirty-percent (n = 15/48) of studied neurons responded to both passive somatosensory stimulation and to the motor task. A consistent percentage of task-related neurons in SII/pIC was selectively activated during finger exploration (FE) and precision grasping (PG) execution, suggesting they play a pivotal role in control skilled finger movements. Furthermore, hand-manipulation-related neurons also responded when visual feedback was absent in the dark. Altogether, our results suggest that somato-motor neurons in SII/pIC likely contribute to haptic processing from the initial to the final phase of grasping and object manipulation. Such motor-related activity could also provide the somato-motor binding principle enabling the translation of diachronic somatosensory inputs into a coherent image of the explored object.

Functional Properties of Parietal Hand Manipulation–related Neurons and Mirror Neurons Responding to Vision of Own Hand Action

“…Fadiga et al suggested that this modulation is due to an effect along the parietal-frontal pathway. Similar interactions between motor and somatosensory signals have been shown (Ishida, Fornia, Grandi, Umilta, & Gallese, 2013;Gardner, Debowy, Ro, Ghosh, & Babu, 2002). The secondary somatosensory cortex and posterior insula cortex have reciprocal connections with the parieto-premotor grasping-related areas.…”

“…The secondary somatosensory cortex and posterior insula cortex have reciprocal connections with the parieto-premotor grasping-related areas. Neurons in these areas respond both to passive somatosensory stimulation and to the motor task (Ishida et al, 2013). This network should be involved in somatosensory control of grasping.…”

Predictive coding accounts of shared representations in parieto-insular networks

“…In order to assess motor-related properties in the hand region of SII/pIC, Ishida et al (2013) trained monkeys to perform a handmanipulation motor task using three different grip types (retrieving a food morsel from a groove, a cup, or a plate). A set of neurons in the SII/pIC region was only activated during active handmanipulation of the monkey.…”

“…The circuit may tie social space representation and affective touch action representation. Additionally, in terms of affective touch, neurons in the hand region of SII and the adjacent posterior insular cortex (pIC) have selectivity regarding the type of hand-manipulation that represents hand motor components during grooming, handfinger exploration, and precision grasping (Ishida et al, 2013). Furthermore, the insular cortex is the center of the integration between exteroception (e.g., CT afferents) and interoception, and it interfaces with the limbic system (Mufson et al, 1981;Mufson, 1982a, 1982b;Chikama et al, 1997;Saleem et al, 2008).…”

The role of tactile afference in shaping motor behaviour and implications for prosthetic innovation

“…Neurones in the S2 have been found to process not just somatosensory information, but also actions in object manipulation, specifically in the stages of motor hand grasping (Ishida et al, 2013), suggesting a role in haptic integration. The S2 also appears to encode more cognitive aspects of tactile processing, such as having representations of present and past sensory information, modulations with attention, comparisons between stimuli, correlations with behavioural decisions, and tactile discrimination learning (Hsiao et al, 2002;Murray and Mishkin, 1984;Romo et al, 2002a;Romo et al, 2002b).…”