Abstract
The representations of the surfaces of the hand in the primary somatosensory cortical field, area 3b, were reconstructed in detail in seven owl monkeys and two squirrel monkeys trained to pick up food pellets from five wells of different sizes. From an early clumsy performance in which several to many retrieval attempts were required for each successful pellet retrieval, the monkeys exhibited a gradual improvement in digital dexterity as shown by significant decreases in mean numbers of grasp attempts/successful retrieval and corresponding standard deviations (e.g. 5.8 +/- 4.5 and 4.8 +/- 3.1 respectively, for the smallest well) between the first and last training sessions. All monkeys commonly used alternative, specific retrieval strategies involving various combinations of digits for significant time epochs before developing a highly successful strategy, which, once achieved, was rapidly stereotyped. For example, the numbers of digit combinations used during the first five versus the last five training sessions decreased from 3.3 +/- 0.7 to 1.8 +/- 0.6 for the smallest well. In both owl and squirrel monkeys, as the behavior came to be stereotyped, monkeys reliably engaged limited surfaces of the glabrous tips of two digits (in eight monkeys), or of three digits (in one monkey) in the palpation and manipulation of these small pellets for their location, capture, and transportation to the mouth. In cortical area 3b, the magnification of representation of these differentially engaged glabrous fingertip surfaces was nearly 2x larger than for the corresponding surfaces of other hand digits, or for the contralateral cortical representations of the same digit surfaces on the opposite hand. In parallel, cutaneous receptive field for area 3b neurons representing crucial digital tip surfaces were less than half as large as were those representing the corresponding surfaces of control digits. Receptive field overlaps were smaller on the trained fingertips than on control fingers. Moreover, the proportion of small overlaps was greater for the trained digits (76 +/- 7%) than for the other digits of the same hand (49 +/- 5.4%). There was still a simple, single--but apparently topologically expanded--representation of these differentially engaged skin surfaces in these monkeys. Thus, with very limited manual exercise over a total period of a few hours of practice at a skill played out in brief daily sessions over a several week long training period, the representations of skin surfaces providing information crucial for successfully performing a small-object retrieval behavior appeared to be substantially remodeled in the most 'primary' of the SI somatosensory cortical fields, cortical area 3b. By that remodeling, behaviorally important skin surfaces were represented in a much finer representational grain than normal. Some implications of these findings for motor skill acquisition are discussed.
Highlights
Our objective in the present experimental series was to document the plasticity of the cortical representations of different skin surfaces engaged in the progressive development of this simple motor skill acquisition, as a part of determining how changes in the representations of these engaged skin surfaces in cortical areas 3b, 3a, 1, 2 and SII might contribute to progressive improvements in digital dexterity
How do these Cortical Changes Relate to the Evolution of this Simple, Practiced Motor Skill?. These studies further demonstrate experience-driven cortical plasticity paralleling motor skill acquisition. They show that as a monkey practices a given, specific strategy for small-object retrieval, that behavior results in task-specific changes in one of the cortical representations of sensory inputs that contribute to this progressively refined movement ability
Some simple aspects of this learning-induced representational plasticity for sensory feedback information in a single somatosensory cortical area, area 3b, have been documented. With these cortical representational changes, the specific finger surfaces that have been engaged in the manipulation and grasping of these small spherical objects have come to be represented with about a 2× greater spatial resolution than was the case just a few days and a few hundred practice events earlier
Summary
We have shown that the details of the cortical representations of the hand surfaces in adult monkeys are modified by behavioral training in which restricted sectors of the hand are engaged by a behavioral task (Jenkins et al, 1990, 1993; Recanzone et al, 1992a–d; Wang et al, 1994, 1995). Significant differences in cortical territories of representation, in cortical magnification (area of representation/skin surface area), in receptive field sizes and in some aspects of local representational topography were recorded for these specific skin surfaces that were directly engaged by monkeys successfully performing this small-object retrieval task under difficult task conditions. These substantial changes in cortical field 3b, again, were recorded with training that was limited to a total period of a few hours extending across a small number of brief daily ‘practice’ sessions
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