Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus

Abstract

Despite the tight coupling between sensory and motor processing for fine manipulation in humans, it is not yet totally clear which specific properties of the fingers are mapped in the precentral and postcentral gyrus. We used fMRI to compare the morphology, connectivity and encoding of the motor and tactile finger representations (FR) in the precentral and postcentral gyrus of 25 five-fingered participants (8 females). Multivoxel pattern, structural and functional connectivity analyses demonstrated the existence of distinct motor and tactile FRs within both the precentral and postcentral gyrus, integrating finger-specific motor and tactile information. Using representational similarity analysis, we found that the motor and tactile FRs in the sensorimotor cortex were described by the perceived structure of the hand better than by the actual hand anatomy or other functional models (finger kinematics, muscles synergies). We then studied a polydactyly individual (i.e., with a congenital 6-fingered hand) showing superior manipulation abilities and divergent anatomical-functional hand properties. The perceived hand model was still the best model for tactile representations in the precentral and postcentral gyrus, while finger kinematics better described motor representations in the precentral gyrus. We suggest that, under normal conditions, i.e. in subjects with a standard hand anatomy, the sensorimotor representations of the five fingers in humans converge towards a model of perceived hand anatomy, deviating from the real hand structure, as the best synthesis between functional and structural features of the hand.Significance statement:Distinct motor and tactile finger representations exist in both the precentral and postcentral gyrus, supported by a finger-specific pattern of anatomical and functional connectivity across modalities. At the representational level, finger representations reflect the perceived structure of the hand, which might result from an adapting process harmonizing (i.e., uniformizing) the encoding of hand function and structure in the precentral and postcentral gyrus. The same analyses performed in an extremely rare polydactyly subject showed that the emergence of such representational geometry is also found in neuromechanical variants with different hand anatomy and function. However, the harmonization process across the precentral and postcentral gyrus might not be possible due to divergent functional-structural properties of the hand and associated superior manipulation abilities.

Biases in hand perception are driven by somatosensory computations, not a distorted hand model

“…Crucially, two recent human fMRI studies found that multivariate patterns of neural activity in S1 significantly correlate with the spatial features of the hand and even more so with the spatial features of biased hand perception. 31,32 In this context, these studies suggest that the Bayesian computations that produce geometric finger distortions occur in early somatosensory cortical processing. We hypothesize that the integration of the spatial likelihood and prior is implemented in S1, perhaps through biases in tuning curve distributions 33 and/or neural population dynamics.…”

“…48 Furthermore, two recent human fMRI studies reported that activity in S1 correlates with the spatial features of the hand and biases in hand perception, as if it embeds a spatial prior. 49,50 In neurocomputational terms, this prior may interact with sensory signals by influencing tuning curve distributions, 51 lateral intraareal connectivity strength, 52 and/or neural population dynamics. 53 Another possibility is that the Bayesian computation is more distributed and may include other regions.…”

Exploring potential neuroimaging biomarkers for the response to non-steroidal anti-inflammatory drugs in episodic migraine

“…The INS is a hub in the SN, which is mainly responsible for regulating attention shifting between the exogenous and endogenous states [ 45 – 47 ]. The PoCG belongs to the primary sensory cortex (S1) and combines the premotor cortex, primary motor cortex, and posterior parietal cortex to receive and integrate motor and sensory information for planning and coordinating complex movements [ 48 , 49 ]. The TTG also known as Heschl’s gyrus is the typical location of the primary auditory cortex and is the first cortical structure to process incoming auditory information [ 50 ].…”

“…The INS is a hub in the SN, which is mainly responsible for regulating attention shifting between the exogenous and endogenous states [45][46][47]. The PoCG belongs to the primary sensory cortex (S1) and combines the premotor cortex, primary motor cortex, and posterior parietal cortex to receive and integrate motor and sensory information for planning and coordinating complex movements [48,49].…”

A roadmap for implanting microelectrode arrays to evoke tactile sensations through intracortical microstimulation

“…The latero-medial organization from the thumb to the little finger in somatosensory cortex was originally observed by Penfield using intraoperative electrical stimulation of humans 24,25 and has been confirmed in multiple species [26][27][28][29][30] including non-human primates [18][19][20]31 . This somatotopic finger organization can also be observed in humans using non-invasive imaging techniques -functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) [32][33][34][35][36][37][38][39][40] . Importantly, several studies have demonstrated highly preserved finger representations in people who were deafferented through amputation [41][42][43][44] or spinal-cord injury (SCI) 45 ; the two groups of people most likely to benefit from BCIs to restore upper limb function.…”