Large-scale expansion of the face representation in somatosensory areas of the lateral sulcus after spinal cord injuries in monkeys

Abstract

Transection of dorsal columns of the spinal cord in adult monkeys results in large-scale expansion of the face inputs into the deafferented hand region in the primary somatosensory cortex (area 3b) and the ventroposterior nucleus of thalamus. Here, we determined whether the upstream cortical areas, secondary somatosensory (S2) and parietal ventral (PV) areas, also undergo reorganization after lesions of the dorsal columns. Areas S2, PV, and 3b were mapped after long-term unilateral lesions of the dorsal columns at cervical levels in adult macaque monkeys. In areas S2 and PV, we found neurons responding to touch on the face in regions in which responses to touch on the hand and other body parts are normally seen. In the reorganized parts of S2 and PV, inputs from the chin as well as other parts of the face were observed, whereas in area 3b only the chin inputs expand into the deafferented regions. The results show that deafferentations lead to a more widespread brain reorganization than previously known. The data also show that reorganization in areas S2 and PV shares a common substrate with area 3b, but there are specific features that emerge in S2 and PV.

Figure 1.

Location of area S2 and PV in macaque monkeys. A, A dorsolateral view of the macaque brain showing locations of the lateral sulcus (LS), intraparietal sulcus (IPS), and central sulcus (CS). The dashed line marks the location from where the section shown in B was taken. The rectangle demarcates the area of the cortex shown in a flattened view in C. B, Drawing of a section from the brain showing locations of area 3b (stippled) in the posterior bank of CS, and areas S2 and PV (hatched) in the upper and inner bank of LS. The primary auditory cortex (Aud) is labeled for reference. The colored regions between sulcal landmarks correspond to the similarly colored regions in C. The dashed line marks the middle of layer 4. C, Flattened view of part of the cortex shown bounded by the rectangle in A. This flattened view was reconstructed from drawings of the brain sections such as the one shown in B. The line corresponding to the medial lip of LS is drawn as a straight line. For details of the flattening procedure, see Materials and Methods. The dashed vertical line marks the location from where the section shown in B was taken. The arrows marking the directions are also valid for A. R, Rostral; M, medial. D, A composite of photomicrographs of cytochrome oxidase-stained sections of the cortex through CS and LS from monkey LM31. The cortex was cut at an angle approximately perpendicular to the lateral sulcus (see dashed line in A). The arrows point to small electrolytic lesions made to help determine the angle of the electrode tracks. Area 3b and the primary auditory cortex (Aud) are easily seen because of a darkly stained, prominent layer 4. Area 4 or the primary motor cortex (M1), area 3a, and area 1 are also marked. These areas were demarcated using adjacent sections stained for Nissl substance, acetylcholine esterase, or myelin. This section was caudal to the section outlined in B.

Figure 2.

Organization of areas S2 and PV in a normal adult macaque monkey, NM116. A, Areas S2 and PV (shaded in light gray) have a medial-to-lateral sequential representation of the face, hand/arm, trunk, and lower limb. The border between area S2 and area PV is marked by a dashed line. The thick gray lines depict the lips and the fundus of various sulci (Fig. 1C). The thin black lines mark boundaries between representations of different body parts, as labeled. The region shaded in dark gray corresponds to the face representation. B, Reconstruction of the cortical surface as in A showing recording sites. The large dots mark the sites in which neurons responded to tactile stimulation, and small dots mark nonresponsive sites. The stippled area in the lower bank of the lateral sulcus is the core region of the auditory cortex (Aud) that was delineated from sections stained for acetylcholine esterase. Conventions are as for Figure 1.

Figure 3.

Reorganization of areas 3b, S2, and PV in monkey LM31. A, Flattened view of the cortex that includes area 3b and S2/PV (Fig. 1). The normal face representation in area 3b and the surrounding cortex, and area S2/PV is shown in pink. Note the expansion of the face representation in area 3b as well as S2/PV (regions shaded in orange). The expected normal hand–face border in area 3b is marked by a blue arrowhead. Note that, in this view, the caudal lip of the central sulcus is toward the bottom part of the figure. B, Location of recording sites in area 3b and S2/PV. C, Extent of the spinal cord lesion shown in a coronal view. The vertical dashed line marks the midline. NR, No response; UA, upper arm. For other conventions, see Figure 1.

Figure 4.

Reorganization of areas S2 and PV in monkey LM34. A, Note the expanded representation of the face throughout S2/PV (region shaded in orange). B, Location of the recording sites. C, The extent of the spinal cord lesion shown in a coronal view. Outline of the gray matter on the left side is shown for reference. The horizontal line marks the location from where the section shown in D was taken. D, A composite of dark-field photomicrographs of a horizontal section of the spinal cord showing the lesion site (arrow). The dashed line marks the midline. Conventions are as for Figures 1 and 3.

Figure 5.

Reorganization of areas 3b and S2/PV in monkey LM01. A, A reconstruction of the posterior bank of the central sulcus showing the somatotopic map in area 3b and the surrounding cortex. Note the expanded face representation (shaded in orange) in the deafferented hand region. Normal location of the hand–face border is marked by a blue arrowhead on the top. The regions in which neurons responded to touch on the hand as well as the face are hatched with an orange background. A more medial partially mapped portion of area 3b with expansion of the face is not shown. B, Somatotopy in area S2/PV showing expansion of the face representation (shaded in orange). The medial face area (pink) is at the normal expected location of the face representation. Note large regions with responses to tactile stimulation of the hand, which were present because of considerable sparing of the dorsal columns. C, Location of all the recording sites in area S2/PV. D, Extent of the lesion shown in a coronal view of the spinal cord. Conventions are as for Figures 1 and 3.

Figure 6.

Comparison of receptive fields of neurons in the expanded face representation in areas 3b and S2/PV. A, Region of the face covered by receptive fields in the deafferented parts of area 3b of all the three monkeys with dorsal column lesions. Note that, in area 3b, only chin inputs expand. B, Figurines showing different kinds of receptive fields on the chin in the deafferented parts of area 3b of the three monkeys. If the same receptive field was encountered multiple times, it is shown only once. C, Region of the face covered by all the receptive fields in the reorganized part of area S2/PV in all the three monkeys. The top figurine shows combined receptive fields that were entirely on the chin; middle figurines, the composite of receptive fields that were on the chin but also extended to the other parts of the face; and bottom figurines, the receptive fields that excluded the chin. D, Different kinds of receptive fields on the face in the reorganized parts of area S2/PV in the three monkeys. Receptive fields at the same location encountered more than once are not shown separately.

Figure 7.

Receptive fields on the hand in areas 3b and S2/PV of normal and lesioned monkeys. A, B, Examples of receptive fields on the hand in area 3b of two normal monkeys (A) and three monkeys with lesions of the dorsal columns (B). Note that the receptive fields in the lesioned monkeys are large. C, D, Receptive fields of neurons in areas S2 and PV of normal monkeys (C) and lesioned monkeys (D) are of similar sizes. E, F, The ratio of the average size of the hand receptive fields in the lesioned and the normal monkeys for area 3b and area S2/PV, respectively. The dashed lines correspond to the ratio of 1. Note different scales for the y-axes in E and F. *p < 0.05; ***p < 0.001; NS, not significant.

Figure 8.

A schematic showing large-scale reorganization at different levels in the somatosensory system after lesions of the dorsal columns. Expansion of the face inputs into the hand region has been observed in the VP nucleus of thalamus, area 3b, and areas S2 and PV. A nearly complete “filling in” of the deafferented regions was observed in the VP nucleus and area 3b, whereas the expansion was patchy in areas S2 and PV. It is presently not known whether there is a similar expansion of the face inputs into the cuneate nucleus of the brainstem, although growth of afferents from the trigeminal nucleus into the cuneate nucleus has been shown (see Discussion). The outline color indicates the expected representation (blue, hand; red, face) and the fill color shows the observed representation after lesions of the dorsal columns (pink, normal face; orange, expanded face). The solid arrows show lemiscal inputs; the dashed arrows indicate the intact spinothalamic inputs via the VPI nucleus and the equivalent inputs from the face. The thin dashed lines indicate weaker inputs. The overall convergence and divergence of the inputs is much more extensive than shown here. For additional details and references, see Discussion.