Analysis of haptic information in the cerebral cortex

K. Sathian
2016 Journal of Neurophysiology  
17 Haptic sensing of objects acquires information about a number of properties. This review 18 summarizes current understanding about how these properties are processed in the cerebral 19 cortex of macaques and humans. Non-noxious somatosensory inputs, after initial processing in 20 primary somatosensory cortex, are partially segregated into different pathways. A ventrally 21 directed pathway carries information about surface texture into parietal opercular cortex and 22 Primates, including
more » ... ns, use the hand to grasp objects not only to act on them, but also, 34 importantly, to acquire sensory information that serves both perceptual and motor goals. 35 Termed "haptic", such sensing covers a variety of object features, including object shape, size, 36 weight, surface texture, compliance and thermal characteristics (Sathian, 1989). It is well known 37 that the visual system gathers information about a host of properties of objects and the 38 environment and parses this information for processing in different visual cortical areas. 39 Similarly, somatosensory information acquired haptically is also subjected to detailed analysis. 40 Although considerably less is understood with regard to the central neural processing of haptic 41 compared to visual sensory information, a good deal of progress has been made over the past 42 few decades. This review focuses on the current state of knowledge about the analysis of haptic 43 inputs in the neocortex, based on neuroimaging studies in humans and neurophysiological 44 studies in non-human primates. Gaps in knowledge and opportunities for future work are 45 highlighted. While the focus is on neocortical information processing, the discussion is framed 46 against the background of work in psychophysics and peripheral afferent neurophysiology. 47 NEOCORTICAL REGIONS PROCESSING SOMATOSENSORY INFORMATION 49 The explosion of interest in multisensory processing has led to increasing appreciation that 50 much of sensory cortex is multisensory, even regions traditionally regarded as unisensory 51 (Ghazanfar and Schroeder, 2006). Thus, somatosensory information is handled not only in 52 classical somatosensory areas, but also outside them (Lacey and Sathian, 2015). A number of 53 neocortical regions process non-noxious haptic inputs, including primary somatosensory cortex 54 (S1), parietal opercular cortex, parts of posterior parietal cortex, and visual cortical areas. Figure 55 1 illustrates these neocortical areas in the human brain, while Figures 2 and 3 diagram their 56 relationship in the context of specific object properties. 57 58 Primary somatosensory cortex 59 S1, located in the postcentral gyrus, comprises four distinct cytoarchitectonic fields: from 60 anterior to posterior, these are Brodmann's areas (BAs) 3a, 3b, 1 and 2 (Figure 1). BA 3a is 61 located in the depths of the central sulcus at the transition between the postcentral and 62 precentral gyri while BA 3b occupies the posterior bank of the central sulcus. BA 1 forms the 63 crown of the postcentral gyrus and continues into BA 2 more posteriorly. In a classic article, 64 Kaas et al. (1979) reported the existence of separate representations of the body in BAs 3b, 1, 65 and 2, and probably 3a as well, in both New World (owl, squirrel and capuchin) and the 66 evolutionarily more recent Old World (macaque) monkeys. The BA 3a map was later confirmed 67 in macaques (Krubitzer et al., 2004). BAs 3b and 1 responded to cutaneous stimuli, whereas BA 68 3a appeared to be primarily responsive to deep stimuli, consistent with it being the target of 69 muscle spindle afferents. BA 2 was activated by deep stimuli, and was additionally responsive 70 to cutaneous stimuli in macaque but not owl monkeys. A recent report (Kim et al., 2015) 71 challenges the idea of strictly segregated processing of cutaneous and proprioceptive input 72 within the macaque hand representation in BAs 3a, 3b and 1. In this study, proprioceptive 73 responses were found in all four sub-fields of S1, being most frequent in BA 3a (72%), least 74 frequent in BA 3b (32%) and intermediate in BAs 1 and 2 (just over 50%). Further, about half of 75 S1 neurons received convergent cutaneous and proprioceptive input from the hand (Kim et al., 76 2015). This fits with the finding that each subdivision of S1 receives convergent thalamic input 77 from multiple nuclei, including the main ventral posterior nucleus with its well-established lateral 78 and medial subdivisions, the ventral posterior superior and ventral posterior inferior nuclei, the 79 posterior division of the ventral lateral nucleus and the anterior pulvinar nucleus, while each of 80 these thalamic nuclei provides divergent input to multiple fields of S1 (Padberg et al., 2009). 81 Interestingly, linear summation of cutaneous and proprioceptive inputs is observed at the time of 82 first response in S1 neurons, whereas nonlinear integration of these inputs only emerges 80 ms 83 later, implying involvement of further neural processing (Kim et al., 2015). Cooling BAs 5 and 7b modified neuronal responses, including RF sizes, in BAs 1 and 2 (Cooke 131 et al., 2014; Goldring et al., 2014), implying the existence of feedback signals to S1 from 132 posterior parietal areas. Although homology between macaque and human parietal cortical 133 regions remains presumptive, probable human counterparts of many of the macaque IPS 134 regions have been identified (Grefkes and Fink, 2005), including the anterior, medial, lateral, 135 ventral, and caudal (posterior) intraparietal areas (AIP, MIP, LIP, VIP and CIP, respectively). 157 resonance imaging (fMRI) in humans has demonstrated segregation of somatosensory 158 information flow into two pathways, one dorsally directed and the other ventrally directed. 159
doi:10.1152/jn.00546.2015 pmid:27440247 pmcid:PMC5144710 fatcat:khwuwcltdba3vpf7xsvedodw3i