522 Hierarchical somatosensory Yoshiaki lwamura processing Recent studies of the postcentral and additional somatosensory cortices support a hierarchical scheme for information processing. In the postcentral gyrus, the complexity of receptive field properties increases with caudal progression from area 1. It has been reported that the anterior bank of the intraparietal sulcus, the caudalmost part of the postcentral gyrus, is responsible for the systematic integration of bilateral body parts, as well as of somatic and visual information. Addresses Department of Physiology, Toho University School of Medicine, 5-21-16 Omori-Nishi, Otaku, Tokyo, Japan 143-8540; e-mall: [email protected] Current Opinion in Neurobiology 1998, 8:522-528 http://biomednet.com/elecref/0959438800800522 0 Current Biology Publications ISSN 0959-4388 Abbreviations fMRl functional magnetic resonance imaging IPS intrapartetal sulcus PET positron emission tomography RF receptive field SI first somatosensory cortex SII second somatosensory cortex SEF somatosensory evoked magnetic field SEP somatosensory evoked potential Introduction In this review, I will describe the hierarchy involved in information processing within the first somatosensory cortex (areas 3a, 3b, 1 and 2) and area 5 in the postcentral gyrus. I will also discuss the second somatosensory cortex (SII) and surrounding areas in the lateral sulcus, and area 7b in the lateral parietal association cortex. While recording from the somatosensory cortex, there is a systematic increase in the complexity of neuronal reccptivc field (RF) properties when the recording site is moved caudally. It is assumed that this increase in com- plexity results from the convergence of multiple inputs onto single neurons via serial cortico-cortical connections and additional thalamic projections. The presence of hierarchical processing in the postcentral somatosensory cortex was first suggested by Duffy and Burchfirl [l] and by Sakata et crl. [Z] on the basis of single-unit recording studies in the monkey. They showed that RFs of area 5 neurons (both skin and joint) tend to be larger and more complex than those in the first somatosensory cortex (SI), and postulated that the complexity of area 5 neurons was attributable to the convergence of simple RF information from neurons in SI. Later, Hyvarinen and Porancn [3] showed that the increase in the size and complexity of cutaneous RFs does in in fact start in area 1. Complex types of neuronal responses have been found in areas 1 and 2 [4,5], and overlapping representation of different digits has been reported in area 2 [6]. Since then, much knowledge has accumulated to support a hierarchical scheme in this cortical region [7,8]. The serial cortico-cortical relationships between these cortical areas have been well documented anatomically 18-131. IIere, I will briefly describe the results of these earlier studies, as well as the results of more recent studies that lend support to a hierarchical scheme. I will also try to interpret the results from other studies in the somatosensory cortex in light of this scheme. In my opinion, many of the recent important papers wcrc published in 1996. Receptive field complexity increases along the anterior-posterior axis of the postcentral gyrus In SI of primates, direct thalamocortical affercnt fibers from the ventrobasal complex project mainly to either area 3b (cutaneous inputs) or area 3a (deep inputs). As area 3a is morphologically a transitional zone from the motor to the sensory cortex, it is difficult to define anatomi- cally. A recent study in human brain has demonstrated that the cytoarchitectonic border between arcas 3a and 4 coincides with changes in the distribution patterns of various neurotransmitters and that the ligand-binding patterns of areas 3a and 3b are similar, supporting the somatosensory nature of arca 3a [ 14’1. In the digit region of area 3b, functionally unique parts of digits (i.e. tips, ventral glabrous surfaces, and dorsal surfaces) are represented separately and independently from each other, forming different subdivisions of area 3b [15]. In the subdivision representing digit tips, the RFs are smaller and more variable than in other subdivisions. The interdigital integration seen in the more caudal parts of the gyrus originates from an initial categorization within area 3 [16,17]. A recent anatomical study [lH] challenges the hypothesis that the intcrareal connections dircctl) create RF enlargement, particularly in area 1, bccausc the connections between areas 3b and 1 are weaker than intrinsic ones within area 3b. It should be pointed out, however, that there may be regional differences in extent of interareal connections, as interdigital integration in area 1 occurs more often for ulnar digits than for radial ones [19]. In the caudal part of the gyrus, there are unique neurons that respond selectively to specific features of a stimulus [4,.5,X!]. In the monkey, some of these neurons arc activated better or solely by active hand movements, such as reaching [Zl]. Tremblay et al. [22] have reported thatHierarchical somatosensoty processing lwamura 523 even though texture-related neurons can bc observed in areas 3b. 1 and 2, those in area 2 ha\re no apparent peripheral RFs when tested with a hand-held probe, yet they signal differences in surface texture. Increase in RF complexity toward the caudal part has also been reported in the proximal arm/trunk region [23”]. Even in cats. the RFs of neurons in area 2 are generalI) larger and the response characteristics are often more complex than those in arca 3 [21,2.5]. Observations in favor of serial hierarchical processing The response latency of neurons to a vibration