Functional organization of motor cortex of adult macaque monkeys is altered by sensory loss in infancy

Abstract

When somatosensory cortex (S1) is deprived of some of its inputs after section of ascending afferents in the dorsal columns of the spinal cord, it reorganizes to overrepresent the surviving inputs. As somatosensory cortex provides guiding sensory information to motor cortex, such sensory loss and representational reorganization could affect the development of the motor map in primary motor cortex (M1), especially if the sensory loss occurs early in development. To address this possibility, the dorsal columns of the spinal cord were sectioned between cervical levels (C3-5) 3-12 days after birth in five macaque monkeys. After 3-5 years of maturation (young adults), we determined how movements were represented in M1 contralateral to the lesion by using microelectrodes to electrically stimulate sites in M1 to evoke movements. Although the details of the motor maps in these five monkeys varied, the forelimb motor maps were abnormal. The representations of digit movements were reduced and abnormally arranged. Current levels for evoking movements from the forelimb region of M1 were in the normal range, but the lowest mean stimulation thresholds were for wrist or elbow instead of digit movements. Incomplete lesions and bilateral lesions produced fewer abnormalities. The results suggest that the development of normal motor cortex maps in M1 depends on sensory feedback from somatosensory maps.intracortical microstimulation | motor map | primate | sensory deprivation | spinal cord injury S ensory guidance plays an important role in movement control.When the somatosensory afferents from the forearm are removed or reduced in number by section of the dorsal roots or dorsal columns, monkeys become reluctant to use the affected forelimb, although they can be trained to do so (1-3). This reluctance to use the affected limb can largely be attributed to sensory loss. However, when the sensory loss is incomplete, the somatosensory system reorganizes over time so that cortical neurons deprived of their normal sources of activation become responsive to preserved somatosensory inputs (3-7). Most notably, a partial loss of inputs from the hand is followed by the reactivation of deprived parts of somatosensory cortex (area 3b) by preserved inputs from the hand, and even inputs from the face over longer periods of recovery. This reactivation produces a distorted sensory map in area 3b that no longer represents some parts of the hand and overrepresents others. This distorted map relays less than optimal sensory information to higher order sensory representations (8) and then to motor cortex, possibly altering the somatotopy of the motor representation in developing or even mature monkeys. Postlesion changes in the cortical motor map could reflect an altered use of the hand after the sensory loss, as motor cortex organization is shaped by experience (9).Here we used electrical microstimulation techniques to study the organization of primary motor cortex of young adult macaque monkeys reared from infancy with a sensory loss produced by a le...

Impairment and recovery of hand use after unilateral section of the dorsal columns of the spinal cord in squirrel monkeys

“…Partial recovery of response properties in M1 to sensory stimulation parallels recovery of hand dexterity [11]. Dorsal column section also compromises the topographic organization of movements in M1 as determined with microstimulation [54, 55]. Given that the motor outputs are preserved, distortions in the motor map may be related to somatotopic reorganization in area 3b and other somatosensory areas.…”

The origins of thalamic inputs to grasp zones in frontal cortex of macaque monkeys

“…However, some electrical stimulation sites that evoked grasping were identified as far rostral as the border separating M1 from premotor cortex. Although the anterior bank of the central sulcus was not mapped, physiological and anatomical evidence suggests the existence of a contiguous representation of the digits in the same medio-lateral extent (Qi et al 2000, 2010; Rathelot and Strick 2009). In three cases, electrical stimulation extended sufficiently rostral and lateral from the M1 grasp zone where a separate grasp zone was identified in PMv (Fig.…”

“…Thus, converging evidence indicates that our M1 grasp zone overlaps part of the hand representation that is involved in grasping. Although the anterior bank of the central sulcus was not systematically explored here, anatomical (Dum and Strick 1991; Rathelot and Strick 2009) and neurophysiological (Park et al 2001, 2004; Qi et al 2000, 2010; Schieber 2001) approaches reveal a substantial representation of the digits. Thus, long train electrical stimulation within this approximate territory of the anterior bank of the central sulcus could be expected to evoke grasping movements.…”

Cortical reorganization after spinal cord injury: Always for good?

“…In monkeys, dorsal column lesions within the first two weeks after birth lead to functional reorganization of the motor cortex in adulthood, uncovering the potential for motor reorganization due to loss of focal sensory inputs (Qi et al, 2010). In cats (McKinley and Smith, 1990) and rats (Jain et al, 1995), as described above, spinal cord injuries inflicted during adulthood are associated with little or no responsiveness in the deafferented cortex.…”