Representational plasticity in cortical area 3b paralleling tactual-motor skill acquisition in adult monkeys

The representations of the surfaces of the hand in the primary somatosensor y cortical field, area 3b, were reconstructed in detail in seven owl monkey s 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 ma ny retrieval attempts were required for each successful pellet retrieval, t he monkeys exhibited a gradual improvement in digital dexterity as shown by significant decreases in mean numbers of grasp attempts/successful retriev al 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 se ssions. All monkeys commonly used alternative, specific retrieval strategie s involving various combinations of digits for significant time epochs befo re developing a highly successful strategy, which, once achieved, was rapid ly 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 +/- for the smallest well. In both owl and squirrel monkeys, a s the behavior came to be stereotyped, monkeys reliably engaged limbed surf aces of the glabrous tips of two two digits tin eight monkeys), or of three digits tin one monkey) in the palpation and manipulation of these small pe llets for their location, capture, and transportation to the mouth. In cort ical area 3b, the magnification of representation of these differentially e ngaged glabrous fingertip surfaces was nearly 2x larger than for the corres ponding surfaces of other hand digits, or for the contralateral cortical re presentations 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 c orresponding surfaces of control digits. Receptive field overlaps were smal ler on the trained fingertips than on control fingers. Moreover, the propor tion 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 simp le, single - but apparently topologically expanded - representation of thes e differentially engaged skin surfaces in these monkeys. Thus, with very li mited manual exercise over a total period of a few hours of practice at a s kill played out in brief daily sessions over a several week long training p eriod, the representations of skin surfaces providing information crucial f or successfully performing a small-object retrieval behavior appeared to be substantially remodeled in the most 'primary' of the SI somatosensory cort ical fields, cortical area 3b. By that remodeling, behaviorally important s kin surfaces were represented in a much finer representational grain than n ormal. Some implications of these findings far motor skill acquisition are discussed.