Patterns of cortical reorganization in the adult marmoset after a cervical spinal cord injury

Abstract

In the present study, we used microelectrode recordings of multiunit responses to evaluate patterns of the reactivation of somatosensory cortex after sensory loss produced by spinal cord lesions in the common marmoset (Callithrix jacchus). These New World monkeys have become a popular model in studies of cortical organization and function. Primary somatosensory cortex and adjoining somatosensory areas can become extensively deactivated by lesions of somatosensory afferents as they ascend in the dorsal columns of the cervical spinal cord. Six to 7 weeks after complete lesions of the cuneate fasciculus subserving the forelimb at cervical levels 5-6, the hand region in contralateral areas 3b and 1 was reactivated by inputs from the forelimb, but excluded representations of some or all digits. In a similar manner, recording sites from the forelimb region of areas 2-5 responded to parts of the forelimb but not to digits after an extensive lesion of the contralateral cuneate fasciculus at C5-C6. Lesions that damaged only the gracile fasciculus or a small percentage of the cuneate fasciculus did not produce changes in the gross hand representation in contralateral areas 3b, 3a, 1, and 2. Finally, a complete but lower lesion of the cuneate fasciculus at C8 produced some abnormalities in the reactivation, but the digits were represented. The results indicate that areas 3a, 3b, 1, and 2-5 of the somatosensory cortex are extensively reactivated after large, apparently complete lesions of the contralateral cuneate fasciculus, but afferents from the digits may not contribute to their reactivation.

Keywords: New World monkey; cortical plasticity; somatosensory.

Figure 1

A reconstruction of the spinal cord lesion at the cervical C5/C6 level in marmoset 9-28. A: The extent of the lesion (shading) as reconstructed from serial sections cut in the horizontal plane and processed for cytochrome oxidase (CO). The horizontal lines mark the locations of sections shown in B and C. The illustrated lesion includes both missing tissue and the glial scar. B,C: Horizontal sections through the spinal cord stained for CO. Each section is aligned with guidelines (not shown) that intersect the pinpoints and the midline; then the spinal cord width, gray matter, and lesion/glial scar borders are demarcated. The reconstructed spinal cord in this case indicated that a complete lesion of the dorsal columns had been made. Scale bar = 1 mm in B (applies to B,C). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 2

Labeling of the cuneate nucleus by CTB injection into the digits after unilateral dorsal column lesions. A: The distribution of CTB-labeled axon terminals in the cuneate nucleus of marmoset 9-28 after the dorsal columns were sectioned at the C5/C6 level on the left side. All five digit tips were injected in both hands. A lack of label in the left cuneate nucleus, compared with the dense patches of label in the right nucleus, indicated that the lesion successfully interrupted afferents from all five digits. B: Pattern of label after injections of CTB in digits of both hands in four other cases with C5/C6 unilateral dorsal column lesions. Sparse label in the cuneate nucleus on the lesioned side in cases 10-34 and 9-26 indicates that the lesions were large, but incomplete. Scale bar = 0.5 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 3

A lateral view of a marmoset brain with the locations of the representation of the hand indicated in somatosensory areas 3a, 3b, and 1. For reference, the expected locations of the second somatosensory area (S2) and the parietal ventral somatosensory area (PV), as well as primary and secondary visual areas (17 and 18) are included. Primary motor cortex (M) is rostral to area 3a, and area 2 is caudal to area 1. The lateral sulcus (ls) and a shallow superior temporal sulcus (sts) are identified.

Figure 4

Microelectrode recording results from the hand portions of areas 3b, 3a, and 1 of marmoset monkeys 9-28, 10-32, 10-34, and 10-31 after a lesion of the contralateral dorsal columns. Strong multiunit responses are marked by large dots, and smaller dots indicate weaker responses. Unresponsive sites are marked with an X, and stars indicate where small microlesions were placed so results could be related to the cortical architecture later. Note that in case 9-28 a reduced portion of area 3b was responsive to stimulation on the hand, and only digit 5 was represented. Sites in 3b, 3a, and 1 were responsive to parts of the arm. In case 10-32, neurons were activated by stimulation of parts of the arm, whereas some units responded to digits 2–4. In case 10-34, neurons were largely activated by stimulation of parts of the arm. Responses to all digits were found intermingled with sites responsive to stimulation on other parts of the hand and the arm in area 3b. In case 10-31, sites were unresponsive to the digits, whereas sites throughout the hand cortex responded to parts of the arm and chest. Laterally, sites in face cortex responded to face stimulation. Sho, shoulder; Plm, palm; Hnd, hand; Fa, forearm; Wr, wrist; Nck, neck. An arrowhead marks the myelin-light septum that separates the face–hand territories. Scale bar = 1 mm.

Figure 5

Recording results from the region of area 2 plus area 5 6–7 weeks after a nearly complete lesion of the contralateral dorsal columns in case 9-26. Although the somatotopy of this region of cortex has not been described for marmosets, responses from the hand and palm were obtained, but none from the digits. Laterally, sites responsive to the face occurred. Conventions as in Figure 4.

Figure 6

The locations of recording sites (squares) in areas 2 and 5 relative to myelin-dense area 3b in marmoset 9-26. The recording results are shown in Figure 5. A myelin-sparse septum in lateral 3b (horizontal line) marks the normal location of the hand/face border. Note that recordings are clearly caudal to area 1, and in the expected locations of areas 2 and 5. Conventions as in Figure 3. Scale bar = 1 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]