Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas

Abstract

The general view on the functional role of the monkey inferior parietal lobule (IPL) convexity mainly derives from studies carried out more than two decades ago and does not account for the functional complexity suggested by more recent neuroanatomical findings. We investigated this issue by recording multi- and single units in the IPL convexity of two monkeys and characterizing their somatosensory, visual and motor responses, using a naturalistic (ethologically relevant) approach. These properties were then matched with IPL cytoarchitectonic parcellation. A further aim of this study was to describe the general properties and the localization of IPL mirror neurons, until now not investigated in detail. Results showed that each studied cytoarchitectonic subdivision of the IPL (PF, PFG, PG) is characterized by specific sensory and motor properties. A key feature of the recorded motor neurons is that of coding goal-directed motor acts. Motor responses are somatotopically organized in a rostro-caudal fashion, with mouth, hand and arm represented in PF, PFG and PG, respectively, with a certain degree of overlap between adjacent representations. In each subdivision the motor activity is associated with specific somatosensory and visual responses, suggesting that each area organizes motor acts in different space sectors. Mirror neurons have been found mainly in area PFG and their general features appear to be very similar to those of ventral premotor mirror neurons. The present data suggest that the IPL plays an important role in both action organization and action understanding and should be considered part of the motor system.

The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations

“…Mirror neurons are also present in the rostral part of the inferior parietal lobule (Ipl), particularly in area pFG [10][11][12] and the anterior intraparietal area (AIp) 9,13 (FIG. 1).…”

Contextual modulation of mirror and countermirror sensorimotor associations.

“…The few studies of macaque MNs which report detailed congruency analyses all describe substantial proportions (6-30%) of so-called 'noncongruent' (or 'logically-related') MNs which respond to the observation and execution of different actions (di Pellegrino et al, 1992;Gallese et al, 1996;Rozzi et al, 2008). In addition, they indicate that a significant proportion of macaque MNs (15-65%) are 'ambiguous' in that they respond to the observation or execution of multiple actions (di Pellegrino et al, 1992;Ferrari et al, 2003;Gallese et al, 1996;Rozzi et al, 2008;Umilta et al, 2001). Similarly, the study of sensorimotor units in human participants has revealed large proportions of neurons with both non-congruent and ambiguous sensorimotor properties (Mukamel et al, 2010).…”

“…However, there is evidence that sensorimotor ambiguity may be a typical feature of the MNS, and not merely a product of laboratory S-R training. Substantial proportions of macaque MNs (di Pellegrino et al, 1992;Ferrari et al, 2003;Gallese et al, 1996;Rozzi et al, 2008;Umilta et al, 2001) and human sensorimotor units (Mukamel et al, 2010) discharge indiscriminately during the observation of multiple actions, or selectively during the observation and execution of different actions. The resulting sensorimotor ambiguity is challenging for theories which posit that MNs make a functional contribution to action understanding (Rizzolatti & Craighero, 2004;Rizzolatti et al, 1996), imitation (Heyes, 2011;Iacoboni, 2009), or generic action selection (Hickok & Hauser, 2010).…”

“…However, a close reading of the results from single-cell recording indicates that substantial proportions of macaque MNs (di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992;Ferrari, Gallese, Rizzolatti, & Fogassi, 2003;Rozzi, Ferrari, Bonini, Rizzolatti, & Fogassi, 2008;Umilta et al, 2001) and human sensorimotor units (Mukamel, Ekstrom, Kaplan, Iacoboni, & Fried, 2010) discharge indiscriminately during the observation of multiple actions, or selectively during the observation and execution of different actions. These findings suggest that the sight of an action may often excite several different congruent and noncongruent motor representations.…”

Movement Coding at the Mesoscale in Posterior Parietal Cortex

“…Previously, the primate PPC was conceptualized as forming an "intentional map" made of distinct subareas for planning movements of the eye, arm or hand (Andersen and Buneo, 2002). Systematic electrophysiological mapping has also shown the existence of graded topographies along the surface of the inferior parietal lobe in monkeys (Rozzi et al 2008). Specifically, a somatotopic organization was found for various motor responses, with movements of the mouth being most rostral, movements of the hand next, and arm movements most caudal.…”