Digit removal leads to discrepancies between the structural and functional organization of the forepaw barrel subfield in layer IV of rat primary somatosensory cortex

Abstract

The physiological representation of the forepaw in rat primary somatosensory cortex (SI) is topographically organized. This representation is associated with the unique arrangement of barrels in layer IV of the forepaw barrel subfield (FBS) in SI and provides an example of a relationship between cortical structure and function. It has been reported that removal of peripheral afferent input to the FBS prior to postnatal day 5 or 6 results in a disorganized FBS, while deafferentation at later times produces little or no alteration of the FBS. Therefore, restricted deafferentations of individual digits in adult rats should result in little, if any, disruption of the FBS, while at the same time eliminating afferent input to the FBS from a localized region of the periphery. This manipulation is likely to create a mismatch between structure and function and offer insight into what barrels actually represent in the adult deafferent. In the present study, we amputated digit three (D3) in eight adult rats, allowed a 1-month survival time, physiologically mapped the representation of D2, D4, and the stump, and compared this physiological map to the underlying barrels in the FBS. Our results showed that FBS barrels formerly associated with the representation of D3 were now associated with the representation of surrounding digits D2 and D4, as well as the remaining stump. By superimposing the morphological and physiological map upon one another, it was clear that the D2 and D4 representations expanded into the former D3 barrel territory and septae between the barrels. The reorganized physiological map was somatotopically organized, even though the general configuration of the morphological map remained unaltered, as visualized with cytochrome oxidase staining. These results suggest that in the deafferent, neurons within FBS barrels previously associated with the representation of punctate regions of skin become associated with neighboring regions of skin. A morphological substrate to account for this cortical reorganization is described.

Mapping plasticity in the forepaw digit barrel subfield of rat brains using functional MRI

“…Whereas the widths of both D2 and D4 activations did not change, the distance between their peak signals was significantly reduced to 0.9 ± 0.2 mm (p < 0.01, two-tailed unpaired t-test). This is consistent with the literature indicating that the nearby digit representations expand and take over the representation of the amputated digit (McCandlish et al, 1996). This can also be seen from the averaged profiles, crossing the centers of D2 and D4 activations in layer IV, from the correlation coefficient maps (Fig.…”

“…The well-defined relationship between the cortical barrels and the forepaw digits makes this system a good model for the study of neural function and plasticity. For example, it has been reported that removal of a peripheral afferent input to the forepaw barrel subfield prior to postnatal day 5 or 6 results in a disorganized forepaw barrel subfield, whereas deafferentation at later times produces little or no alteration of the forepaw barrel subfield (Dawson and Killackey, 1987; McCandlish et al, 1996). Although the representation of digit columns has been investigated by optical imaging of intrinsic signals (Gochin et al, 1992) and electrophysiological studies (Li et al, 1996; McCandlish et al, 1996), non-invasive mapping remains a challenge.…”

Changes in Intrinsic Properties of Pyramidal Neurons in Adult Rat S1 During Cortical Reorganization

“…The reorganization observed is similar to those observed previously in this system (Hickmott and Merzenich 2002) and in other systems after denervation or amputation (e.g., McCandlish et al 1996;Merzenich et al 1983). A very rapid initial shift in the border was followed by a more protracted shift (Fig.…”

Mapping cortical representations of the rodent forepaw and hindpaw with BOLD fMRI reveals two spatial boundaries

“…A major advantage of using BOLD fMRI for such studies would be the ability to study individual animals longitudinally. Specifically, studies of the changes in the functional boundaries using BOLD fMRI should further studies about the mechanism of neuronal reorganizations (Godde et al, 1996; McCandlish et al, 1996; Melzer et al, 1998; Godde et al, 2002; Calford, 2002). Furthermore, future clarifications of the spatial coupling between the neuronal activity and the physiological phenomena underlying the fMRI BOLD should help advance the understanding of the neuronal basis of fMRI.…”