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.
Highlights
The last 30 years of intensive research has led to a greatly improved understanding of how the somatosensory system of mature primates and other mammals responds to sensory loss, as reviewed by others (Buonomano and Merzenich, 1998; Jones, 2000; Wall et al, 2002; Kaas et al, 2008; Darian-Smith, 2009; Xerri, 2012)
Some changes in the receptive fields of neurons in the somatosensory system were apparent as soon as they could be measured after sensory loss (Wall, 1977; Calford and Tweedale, 1988; Faggin et al, 1997; Xu and Wall, 1997, 1999; Krupa et al, 1999), and these immediate changes could be attributed to the removal of the excitatory drive on central inhibitory neurons that normally constrain the receptive fields of relay neurons by keeping some of the excitatory inputs subthreshold
The remainder of this review mainly focuses on the consequences of dorsal column lesions of the spinal cord in primates, including characteristics of natural recoveries and potential for augmented recoveries, but it is not intended to be a comprehensive literature review of other types of injuries and recovery mechanisms
Summary
The last 30 years of intensive research has led to a greatly improved understanding of how the somatosensory system of mature primates and other mammals responds to sensory loss, as reviewed by others (Buonomano and Merzenich, 1998; Jones, 2000; Wall et al, 2002; Kaas et al, 2008; Darian-Smith, 2009; Xerri, 2012). Receptive field mapping of neurons recorded with a 100-electrode array www.frontiersin.org in area 3b in a squirrel monkey showed that somatotopic organization in reactivated cortex was largely normal after behavioral recovery from a dorsal column lesion at the C6 level (compare Figures 3B,C).
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