A focal zone of thalamic plasticity

Abstract

In this study, sensory maps in the thalamus were investigated by examining their volume and shape. We determined the forelimb representation in adult rats after the removal of hindlimb input by nucleus gracilis lesions. Three-dimensional reconstructions of thalamic sensory maps were obtained from a grid of electrode penetrations. We found that the volume of the shoulder sensory map contracted >50% at an acute time interval (n = 6), followed by a robust volumetric sensory map expansion of 25% at 1 week (n = 8) and 1 month (n = 8) after lesion relative to controls (n = 8). The topology of the volumetric increase was scrutinized by slicing functional maps in the coronal, sagittal, and horizontal planes. The equivalence of such slices from each animal was established by virtue of their distance from either a functional or neuroanatomical landmark. Surprisingly, all of the volumetric increase unequivocally occurred in a circumscribed coronal slice 300 micron thick. This focal zone was located toward the rostral pole of the thalamic tactile relay, the ventroposterolateral nucleus. Analysis in the sagittal plane revealed that, unexpectedly, the shoulder map volume expanded by superimposing its representation on that of the forepaw, via an advancement of the shoulder representation by 0.6 mm medially. We propose a "hot spot" hypothesis in which focal zones of plasticity may not be specific to the thalamus but may have manifestations elsewhere in the nervous system, such as the cerebral cortex or dorsal column nuclei.

Fig. 1.

Sample data from control (top) and lesioned (bottom) animals mapped with vertical electrode penetrations. This is a coronal view of a functional map, depicting classifications of recording sites for all body regions examined (H, hindlimb; F, forepaw;S, shoulder). The forepaw centroid in this plane is the cell with a bold border. For clarity, “blank” recording site designations are omitted.

Fig. 2.

Volume of three thalamic sensory maps at different times after nucleus gracilis lesions. A different group of animals was used for each time point. The recording sites included in the calculation of each sensory map are depicted. Asterisksindicate significant differences between a given treatment group compared with controls. Columns indicate mean; error bars indicate ±SE.

Fig. 3.

A, Coronal plane area of the shoulder sensory map as a function of anteroposterior distance. Maps from each animal are aligned with respect to the anatomically determined anteroposterior midpoint of the VB (anatomical registration). Lateral view of a rat brain indicates the plane of sectioning used on functional shoulder maps. The bar indicates a focal zone of robust change common to both 1 week and 1 month postlesion groups.Asterisks indicate that both 1 week and 1 month postlesion groups are significantly different from controls. Error bars indicate ±SE. B, Coronal plane area of the shoulder sensory map as a function of the anteroposterior distance. Maps from each animal are aligned with respect to the centroid of the forepaw (functional registration). Asterisks indicate that both 1 week and 1 month postlesioned groups are significantly different from controls. Compared with anatomical alignment of coronal slices (A), differences emerge more clearly with the functional alignment. All subsequent planar analysis is on coronal slices corresponding to the focal zone. Error bars indicate ±SE.

Fig. 4.

Spatial distribution of recording sites responsive to shoulder stimulation from control and 1 week postlesion animals. This is a caudal perspective of the sensory map. Lesion-induced changes are most marked at the rostral pole, toward the anterior end of the display. Much of the shoulder expansion appears to occur along the mediolateral axis after gracilis lesions.

Fig. 5.

Plot of residual hindlimb input as a function of the anteroposterior axis. Abscissa coordinates are the same as those in Figure 3B. The area of hindlimb input corresponding to the focal zone relative to the forepaw centroid is indicated by the bar. Asterisks indicate significant differences between all treatment groups compared with control values. Error bars indicate ±SE.

Fig. 6.

Control and 1 week postlesioned animals. Spatial distribution of recording sites that were responsive to hindlimb stimulation are depicted from the caudal vantage point.

Fig. 7.

Cross-sectional area profile of shoulder representation. The focal zone is represented as a dark band in the coronal plane, which was cut sagittally with reference to the intact rat brain. Asterisks indicate significant differences between control versus 1 week and 1 month groups after lesion. As far as 0.6 mm medial to the forepaw centroid, 1 month postlesion was significantly elevated compared with control. Error bars indicate ±SE.

Fig. 8.

Profile of shoulder sensory representation, revealed by cross-sectional slices in the horizontal plane. The focal zone is indicated as a dark coronal band, sectioned with reference to the intact rat brain. Asterisks indicate significant differences for both 1 week and 1 month postlesion groups versus control. Error bars indicate ±SE.

Fig. 9.

Photomicrograph depicting a coronal view of the dorsal column nuclei stained with Nissl 1 week after lesion. The damage observed in the gracile nucleus existed along the length of the nucleus. The accompanying diagram is a schematic rendering of the photomicrograph, barring tissue-processing artifacts. The zone of gliosis is indicated by the stippled area. cu fasc, Cuneatus fasciculus; Cu, cuneate nucleus;Gr, gracile nucleus.

Fig. 10.

Photomicrograph of a 1 month postlesion rat brain sectioned in the horizontal plane and stained with cresyl violet.Arrows are interposed between two rows of electrode penetrations corresponding to the focal zone.

Fig. 11.

Schematic of the topographic overlap between shoulder and forepaw in the focal zone at 1 week and 1 month after lesion. This is a coronal view of forepaw, shoulder, and hindlimb sensory maps in the VPL. The plasticity depicted is derived from data on the volume of shoulder–forepaw overlap (Fig. 2) and planar analysis (Figs. 7, 8).

Fig. 12.

Hot spot model of neural plasticity. A depiction of our identified focal zone or hot spot of reorganization in the thalamus. It is proposed that hot spots exist at other levels of the somatosensory pathway such as the cortex. Cortically, the hot spot is a slice oriented orthogonally to the cortical columns of Mountcastle (1957), in the same way the thalamic hot spot is orthogonally oriented with respect to the thalamic rods of Jones et al. (1979, andJones and Friedman (1982). The somatotopy of the thalamus is rotated compared with that of the cortex, given the difference in the orientation of thalamic rods and cortical columns. See Discussion.