The reactivation of somatosensory cortex and behavioral recovery after sensory loss in mature primates

Abstract

In our experiments, we removed a major source of activation of somatosensory cortex in mature monkeys by unilaterally sectioning the sensory afferents in the dorsal columns of the spinal cord at a high cervical level. At this level, the ascending branches of tactile afferents from the hand are cut, while other branches of these afferents remain intact to terminate on neurons in the dorsal horn of the spinal cord. Immediately after such a lesion, the monkeys seem relatively unimpaired in locomotion and often use the forelimb, but further inspection reveals that they prefer to use the unaffected hand in reaching for food. In addition, systematic testing indicates that they make more errors in retrieving pieces of food, and start using visual inspection of the rotated hand to confirm the success of the grasping of the food. Such difficulties are not surprising as a complete dorsal column lesion totally deactivates the contralateral hand representation in primary somatosensory cortex (area 3b). However, hand use rapidly improves over the first post-lesion weeks, and much of the hand representational territory in contralateral area 3b is reactivated by inputs from the hand in roughly a normal somatotopic pattern. Quantitative measures of single neuron response properties reveal that reactivated neurons respond to tactile stimulation on the hand with high firing rates and only slightly longer latencies. We conclude that preserved dorsal column afferents after nearly complete lesions contribute to the reactivation of cortex and the recovery of the behavior, but second-order sensory pathways in the spinal cord may also play an important role. Our microelectrode recordings indicate that these preserved first-order, and second-order pathways are initially weak and largely ineffective in activating cortex, but they are potentiated during the recovery process. Therapies that would promote this potentiation could usefully enhance recovery after spinal cord injury.

Sensorimotor cortex injury effects on recovery of contralesional dexterous movements in Macaca mulatta

“…Thus, the extent of any sensorimotor deficit is not clear in the F2P2 lesion experiments. However, there was evidence that subjects consistently used vision to verify acquisition of the food targets in these cases, which was also observed in previous studies with somatosensory processing deficits due to spinal dorsal column transection (Qi et al, 2014) or parietal cortex ablation (Kennard and Kessler, 1940). Importantly, the more affected hand of all 6 F2P2 lesion cases was often dragged, with the finger-tips in constant contact with the metal cage floor when moving about the testing cage.…”

Congenital foot deformation alters the topographic organization in the primate somatosensory system

“…The many studies of the somatosensory system in monkeys after various types of sensory loss as adults indicate that the growth of new connections to replace missing or deactivated connections is typical (Darian-Smith 2004; Darian-Smith and Gilbert 1994; Jain et al 2000; Hickmott and Steen 2005), including the activation of hand cortex, and even the hand portion of the CuN and VP after the extensive loss of hand and arm sensory inputs by inputs from parts of the lower face (Florence et al 2000; Jain et al 1997; Pons et al 1991). Thus, the changes in the somatosensory system reported here for the loss of a sensory input due to abnormal development are somewhat similar to those that have been reported after sensory loss in adult monkeys, and the common mechanism in the replacement of missing inputs is by the sprouting and growth of new connections and other potentiation of preserved sensory inputs (Qi et al 2014a; Darian-Smith and Ciferri 2006; Bowes et al 2012). …”

Spatiotemporal trajectories of reactivation of somatosensory cortex by direct and secondary pathways after dorsal column lesions in squirrel monkeys

“…Damage at any level partially reduces the normal source of activation, depriving all subsequent stages of those inputs. Yet, the central nervous system has capabilities to compensate after injury (Buonomano and Merzenich, 1998; Darian-Smith, 2009; Kaas et al, 2008; Qi et al, 2014b; Xerri, 2012). Most studies of deafferentation of ascending somatosensory pathways in primate models have focused on the tactile modality (Chen et al, 2012a; Florence et al, 2000; Florence et al, 1996; Florence et al, 1998; Jain et al, 1997; Merzenich et al, 1983a; Merzenich et al, 1983b; Pons et al, 1991; Qi et al, 2011; Qi et al, 2014a; Vierck and Cooper, 1998; Vierck et al, 1990).…”