Abstract
Focal unilateral injuries to the somatosensory whisker barrel cortex have been shown cause long-lasting deficits in the activity and experience-dependent plasticity of neurons in the intact contralateral barrel cortex. However, the long-term effect of these deficits on behavioral functions of the intact contralesional cortex is not clear. In this study, we used the “Gap-crossing task” a barrel cortex-dependent, whisker-sensitive, tactile behavior to test the hypothesis that unilateral lesions of the somatosensory cortex would affect behavioral functions of the intact somatosensory cortex and degrade the execution of a bilaterally learnt behavior. Adult rats were trained to perform the Gap-crossing task using whiskers on both sides of the face. The barrel cortex was then lesioned unilaterally by subpial aspiration. As observed in other studies, when rats used whiskers that directly projected to the lesioned hemisphere the performance of Gap-crossing was drastically compromised, perhaps due to direct effect of lesion. Significant and persistent deficits were present when the lesioned rats performed Gap-crossing task using whiskers that projected to the intact cortex. The deficits were specific to performance of the task at the highest levels of sensitivity. Comparable deficits were seen when normal, bilaterally trained, rats performed the Gap-crossing task with only the whiskers on one side of the face or when they used only two rows of whiskers (D row and E row) intact on both side of the face. These findings indicate that the prolonged impairment in execution of the learnt task by rats with unilateral lesions of somatosensory cortex could be because sensory inputs from one set of whiskers to the intact cortex is insufficient to provide adequate sensory information at higher thresholds of detection. Our data suggest that optimal performance of somatosensory behavior requires dynamic activity-driven interhemispheric interactions from the entire somatosensory inputs between homotopic areas of the cerebral cortex. These results imply that focal unilateral cortical injuries, including those in humans, are likely to have widespread bilateral effects on information processing including in intact areas of the cortex.
Highlights
Tactile spatial acuity in humans, as well as non-human primates, is said to depend on activity in distributed neural network generated through ‘‘interaction between bottom up tactile inputs and top-down attentional signals’’ (Sathian, 2016)
While learning a somatosensory task, using bilateral somatosensory inputs, activity-dependent plastic changes in somatosensory areas of both hemispheres would be induced due to the reciprocal interhemispheric interactions. This implies that the performance of the task at the highest degree of ability would depend on active somatosensory inputs to both hemispheres
The results imply that learning a tactile behavior modifies the functions of each somatosensory cortex such that the subsequent performance of the learnt behavior at optimal level depends on active bilateral interactions of somatosensory inputs in the somatosensory cortex
Summary
Tactile spatial acuity in humans, as well as non-human primates, is said to depend on activity in distributed neural network generated through ‘‘interaction between bottom up tactile inputs and top-down attentional signals’’ (Sathian, 2016). While learning a somatosensory task, using bilateral somatosensory inputs, activity-dependent plastic changes in somatosensory areas of both hemispheres would be induced due to the reciprocal interhemispheric interactions. This implies that the performance of the task at the highest degree (maximum level) of ability would depend on active somatosensory inputs to both hemispheres. We hypothesized that unilateral lesions would disrupt these bilateral interactions Such disruptions would affect the behavioral functions of the intact contralesional hemisphere due to occurrence of diaschisis (von Monakow, 1914; Carrera and Tononi, 2014), to alter performance of a behavior that was previously learnt using bilateral sensory inputs. The whisker-barrel pathway of the rat is an ideal model system for testing this hypothesis because of vast amount of knowledge available on somatosensory information processing in this system (see recent reviews by Lampl and Katz, 2017; Campagner et al, 2018; Estebanez et al, 2018; Yang et al, 2018)
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