Differential effects of abnormal tactile experience on shaping representation patterns in developing and adult motor cortex

Abstract

This study investigates the influence of early somatosensory experience on shaping movement representation patterns in motor cortex. Electrical microstimulation was used to map bilaterally the motor cortices of adult rats subjected to altered tactile experience by unilateral vibrissa trimming from birth (birth-trimmed group) or for comparable periods that began in adulthood (adult-trimmed group). Findings demonstrated that (1) vibrissa trimming from birth, but not when initiated in adulthood, led to a significantly smaller-sized primary motor cortex (M1) vibrissa representation in the hemisphere contralateral to the trimmed vibrissae, with no evidence for concomitant changes in size of the adjacent forelimb representation or the representation of the intact vibrissae in the opposite (ipsilateral) hemisphere; (2) in the contralateral hemispheres of the birth-trimmed group, an abnormal pattern of evoked vibrissa movement was evident in which bilateral or ipsilateral (intact) vibrissa movement predominated; (3) in both hemispheres of the birth-trimmed group, current thresholds for eliciting movement of the trimmed vibrissa were significantly lower than normal; and (4) in the adult-trimmed group, but not in the birth-trimmed group, there was a decrease bilaterally in the relative frequency of dual forelimb-vibrissa sites that form the common border between these representations. These results show that sensory experience early in life exerts a significant influence in sculpting motor representation patterns in M1. The mature motor cortex is more resistant to the type and magnitude of influence that tactile experience has on developing M1, which may indicate that such an influence is constrained by a developmentally regulated critical period.

Fig. 1.

Surface view maps of M1 vibrissa and forelimb movement representations in adult-control (A), adult-trimmed (B), and birth-trimmed (C) animals. For each group, M1 maps of the left experimental and right hemispheres are shown for two representative animals and illustrate both the individual variation in size and configuration of these movement representations and the effects of vibrissa trimming on the vibrissa representations in the left experimental hemispheres of the birth-trimmed group (C, arrows). The dashed lines betweenleft and right hemispheres represent the positions of the midlines; B, position of bregma;dots, positions of microelectrode penetrations.

Fig. 3.

Comparisons of the mediolateral frequency distribution of penetrations eliciting vibrissa (A) or forelimb (B) movement between adult-control and vibrissa-trimmed groups. For each hemisphere, mediolateral position was distributed into 0.5 mm bins extending from the midline (0 mm) to 5.5 mm lateral of the midline, irrespective of anteroposterior coordinate. The number of penetrations falling into each bin was tallied and expressed as a percentage of the total penetrations (±SEM). The mediolateral distribution of forelimb or vibrissa penetrations was highly variable; statistical comparisons across groups for each bin revealed no significant differences. Thus, vibrissa trimming did not overtly skew the relative positioning of M1 vibrissa and forelimb representations across the mediolateral extent of cortex.

Fig. 2.

Sizes of vibrissa (A) and forelimb (B) representations in left and right hemispheres of control and vibrissa-trimmed groups. Data represent mean values (+SEM). The mean size of the vibrissa representation in the left experimental hemispheres of the birth-trimmed group was significantly smaller in comparison with that of the opposite (right) hemisphere (*p < 0.05, paired Student’s ttest) and with that of the left hemispheres of the other groups (*p < 0.01, ANOVA).

Fig. 4.

Effects of vibrissa trimming on the proportion of contralateral, ipsilateral, and bilateral vibrissa movements evoked from right (A–C) or left experimental (D–F) hemispheres. The pattern of evoked vibrissa output in the right hemispheres was similar across control and vibrissa-trimmed groups (A–C). In contrast, the left experimental hemisphere of the adult-trimmed group (E) displayed a significantly lower proportion of evoked contralateral movement in comparison with controls (*p < 0.05, ANOVA), whereas the proportion of bilateral movements increased slightly but not significantly (p = 0.072). The effects in the left hemisphere of the birth-trimmed group were more pronounced (F). Evoked contralateral movements were infrequent, whereas bilateral movements predominated (*p < 0.0001, ANOVA). Data are mean ± SEM.

Fig. 5.

Across-group comparisons of current thresholds for evoking movement of the trimmed or intact set of vibrissa (vib) from either hemisphere. Current thresholds for evoking movement of the trimmed vibrissa, from either left experimental (A) or right (C) hemispheres, was significantly lower in the birth-trimmed group in comparison with controls (*p < 0.05, ANOVA). Data are means + SEM. contra, Contralateral;ipsi, ipsilateral.

Fig. 6.

Comparisons of current thresholds for evoking contralateral forelimb (A), contralateral hindlimb (B), or jaw (C) movement between controls and vibrissa-trimmed groups. In both hemispheres, current thresholds were similar across groups. Data are means + SEM.

Fig. 7.

Proportion of dual-movement (forelimb and vibrissa) sites in control and vibrissa-trimmed groups. The occurrence of dual-movement sites was expressed as a percentage of total forelimb penetrations. Relative frequency of dual-movement sites was similar between control and birth-trimmed groups but was substantially reduced in both hemispheres of the adult-trimmed group.