Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus

Complex motor responses are often thought to result from the combination of elemental movements represented at different neural sites. However, in monkeys, evidence indicates that some behaviors with critical ethological value, such as self-feeding, are represented as motor primitives in the precentral gyrus (PrG). In humans, such primitives have not yet been described. This could reflect well-known interspecies differences in the organization of sensorimotor regions (including PrG) or the difficulty of identifying complex neural representations in peroperative settings. To settle this alternative, we focused on the neural bases of hand/mouth synergies, a prominent example of human behavior with high ethological value. By recording motor- and somatosensory-evoked potentials in the PrG of patients undergoing brain surgery (2–60 y), we show that two complex nested neural representations can mediate hand/mouth actions within this structure: (i) a motor representation, resembling self-feeding, where electrical stimulation causes the closing hand to approach the opening mouth, and (ii) a motor–sensory representation, likely associated with perioral exploration, where cross-signal integration is accomplished at a cortical site that generates hand/arm actions while receiving mouth sensory inputs. The first finding extends to humans’ previous observations in monkeys. The second provides evidence that complex neural representations also exist for perioral exploration, a finely tuned skill requiring the combination of motor and sensory signals within a common control loop. These representations likely underlie the ability of human children and newborns to accurately produce coordinated hand/mouth movements, in an otherwise general context of motor immaturity.Since Penfield’s original work, it is commonly assumed that complex motor responses are produced by combining elemental movements that are independently represented at different neural sites (1). However, the generality of this model was recently challenged in nonhuman primates, where reaching, grasping, defensive, and hand/mouth movements have been found to be represented as complex motor primitives in independent circumscribed territories of the precentral gyrus (PrG) (2–4). To account for this observation, it was suggested that complex motor primitives have emerged during primate evolution to optimize the production of ethologically relevant behaviors (4). However, to date, direct evidence is lacking that such integrated representations of ethologically relevant movements also exist in humans. This may have two different origins.First, it could be that complex ethologically relevant representations exist in human PrG but have not yet been described, due to the difficulty of identifying neural representations associated with the expression of elaborate sensorimotor behaviors in peroperative contexts. With respect to this point, Penfield and other researchers have clearly reported complex multijoint motor responses following cortical stimulation (5–8), including concurrent movements of the hand and mouth (9). Nevertheless, these movements were not investigated systematically in several subjects, described in detail, or related to the existence of integrated neural representations for ethologically relevant behaviors. An obstacle to the investigation of these representations could have been the tendency to stop the stimulation following movement onset. This was explicitly acknowledged by Penfield in the following terms: “the stimulating electrode has frequently been removed at the first evidence of response, and thus the opportunity of producing more of the elaborate synergic responses may have been missed” (6).At a second level, it could be that the PrG does not contain functional representations of complex ethologically relevant behaviors in humans. This possibility is consistent with the existence of substantial dissimilarities in sensorimotor organization between human and nonhuman primates (10, 11). Interestingly, these dissimilarities are well documented for the precentral region mediating ethological synergies in monkeys. In this species, electrical stimulation in the rostral part of PrG evokes coordinated hand-to-mouth movements (12). These movements are part of the behavioral repertoire of the primate newborns (13), which is consistent with the observation that the rostral (phylogenetically oldest) part of PrG lacks cortico-motoneural cells and generates movements by recruiting the integrative mechanisms of the spinal cord through descending projections that are mature at birth (14). However, in human infants, the difficulty of evoking motor responses through electrical stimulation of the rostral PrG does not seem consistent with the existence of early mature descending projections (15, 16). Also, in adults, transcranial magnetic stimulation studies have suggested, in apparent contrast with monkey data, that late-maturing cortico-motoneural cells are present in the human rostral PrG (17, 18).The main aim of this study was to determine whether integrated neural representations of complex actions can be found in the human PrG. We investigated this possibility by studying the neural bases of hand/mouth synergies, a salient example of early and elaborate human behavior with high ethological value (19–21). To this end, motor and somatosensory mapping were combined in children and adult patients undergoing brain surgeries.