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We investigate the position invariant receptive field properties of neurons in the macaque second somatosensory (SII) cortical region. Previously we reported that many SII region neurons show orientation tuning in the center of multiple finger pads of the hand and further that the tuning is similar on different pads, which can be interpreted as position invariance. Here we study the receptive field properties of a single finger pad for a subset (n = 61) of those 928 neurons, using a motorized oriented bar that we positioned at multiple locations across the pad. We calculate both vector fields and linear receptive fields of the finger pad to characterize the receptive field properties that give rise to the tuning, and we perform an additional regression analysis to quantify linearity, invariance, or both in individual neurons. We show that orientation tuning of SII region neurons is based on a variety of mechanisms. For some neurons, the tuning is explained by simple excitatory regions, simple inhibitory regions, or some combination of these structures. However, a large fraction of the neurons (n = 20 of 61, 33%) show position invariance that is not explained well by their linear receptive fields. Finding invariance within a finger pad, coupled with the previous result of similar tuning on different pads, indicates that some SII region neurons may exhibit similar tuning throughout large regions of the hand. We hypothesize that invariant neurons play an important role in tactile form recognition.

The detailed structure of multidigit receptive fields (RFs) in somatosensory cortical areas such as the SII region has not been investigated previously using systematically controlled stimuli. Recently (Fitzgerald et al., 2004), we showed that the SII region comprises three adjoining fields: posterior, central, and anterior. Here we characterize the RF structures of the 928 neurons that were reported in that study using a motorized oriented bar that was indented into the 12 finger pads of digits 2-5. Most (81%) of the neurons were responsive to the oriented bar stimuli, and 81% of those neurons had RFs that spanned multiple digits. Furthermore, the RFs varied greatly in size, shape, and complexity. Some RFs contained only excitatory finger pads, some contained only inhibitory pads, and some contained both types of pads. A subset of the neurons (23%) showed orientation tuning within one or more pads. The RFs spread across different digits more than within individual digits, and the responsive finger pads for a given neuron tended to cluster together within the hand. Distal and lateral finger pads were better represented than proximal and medial finger pads. Furthermore, neurons in the posterior, central, and anterior SII region fields contained different proportions of RF types. These results collectively indicate that most SII region neurons are selective for different stimulus forms either within single finger pads or across multiple pads. We hypothesize that these RFs represent the kernels underlying the representation of tactile shape.

Orientation tuning has been studied extensively in the visual system, but little is known about it in the somatosensory system. Here we investigate tuning in the second somatosensory (SII) region using a motorized stimulator that presented a small oriented bar to the 12 finger pads of digits 2-5 (D2-D5) of the macaque monkey. A subset (23%; n = 218) of the 928 SII region neurons [the same 928 neurons studied by Fitzgerald et al. (2004, 2006)] exhibited tuning, and most of these were tuned on one or two finger pads. All eight 22.5 degrees separated orientations were represented as the preferred orientation of multiple neurons, although not necessarily in equal numbers. A measure of bandwidth indicated that tuning in the SII region is sharp and is similar to the tuning observed in visual cortical areas. In addition, two-dimensional Gaussians that were fit to the tuning curves had very high r2 values, indicating that most tuning curves are both unimodal and symmetrical with respect to their preferred orientation. Most tuned neurons had additional untuned pads, although the responsiveness of these pads tended to be less than the responsiveness of tuned pads. Neurons with multiple tuned pads tended to have similar preferred orientations on their tuned pads, which can be interpreted as evidence for integration of information across fingers or as a form of positional invariance. Finally, comparison of the tuning properties showed that there are small but significant differences between the posterior, central, and anterior fields of the SII region.

The detailed functional organization of the macaque second somatosensory cortex (SII) is not well understood. Here we report the results of a study of the functional organization of the SII hand region that combines microelectrode mapping using hand-held stimuli with single-unit recordings using a motorized, computer-controlled tactile oriented bar. The data indicate that the SII hand region extends approximately 10 mm in the anteroposterior (AP) dimension, primarily within the upper bank of the lateral sulcus. Furthermore, we find evidence that this region consists of multiple functional fields, with a central field containing neurons that are driven well by cutaneous stimuli, flanked by an anterior field and a posterior field that each contain neurons that are driven well by proprioceptive stimuli and less well by cutaneous stimuli. The anterior field extends approximately 4-5 mm AP, the central field extends approximately 3-4 mm, and the posterior field extends approximately 3 mm. Data from the motorized stimulator indicate that neurons in the central field are more responsive to oriented bars, more frequently exhibit orientation tuning, and have larger receptive fields than neurons in the anterior and posterior fields. We speculate that the three putative fields play different functional roles in tactile perception; the anterior and posterior fields process information that involves both proprioceptive and cutaneous input such as sensorimotor integration or stereognosis, whereas the central field processes primarily cutaneous information.