Learning to see the trees before the forest: reversible deactivation of the superior colliculus during learning of local and global visual features

Abstract

Previous studies have established that deactivation of the superior colliculus severely retards the normally rapid learning of pattern discriminations in the mature cat. The purpose of this study was to test the hypothesis that the midbrain plays an important role in the learning of simple pattern discriminations and that the contribution of this pathway is to the perception of global, rather than local, features of a figure. To answer this question, pattern discrimination learning was studied in three intact cats and in three experimental cats during bilateral reversible deactivation of the superficial layers of the superior colliculus (SC). The animals concurrently learned to discriminate three pairs of compound visual patterns composed of small (local element) Ts or 7s. Congruent and incongruent stimulus pairs were large (global) Ts vs. 7s comprising the same or different local elements, respectively. The random stimulus pair consisted of randomly scattered local elements (Ts vs. 7s). The animals were trained to respond to the large Ts in the congruent and incongruent pairs and the small Ts in the random pair. In the normal cats, learning of the random pair was much slower than the learning of the congruent and incongruent pairs. This finding demonstrated the theory of global precedence, because the animals learned the global features of the congruent and incongruent pairs much more quickly than the local features of the random pair. In contrast, during bilateral deactivation of the superficial layers of the SC, the learning of the incongruent pair was significantly retarded and took longer to learn than the random pair. Congruent and random pair learning rates were unchanged. The specific deficit in learning the incongruent pair indicates that the learning of global, but not local, elements of the visual pattern is impaired during deactivation of the SC. The unimpaired use of local features permitted the animals to learn the congruent and random pairs at normal rates. Therefore, deactivation of the superficial layers of the SC during pattern discrimination learning reverses the precedence for global visual features that is typical of normal learning.

Figure 1

The three discriminations that were concurrently learned. (A) Congruent pair in which both the local and global cues matched. (B) Incongruent pair in which the local and global cues did not match. (C) Random stimulus that consists of only the local cues with no global pattern. Note that these random discriminanda are only an example as the distribution of the local elements changed on each trial. For each stimulus pair, responses to the stimuli in the left column were rewarded. Stimuli were never paired with stimuli of another class. This task was developed originally by Horel (4).

Figure 2

Chart to summarize how specific deficits on the three discrimination pairs (congruent, incongruent, and random) are interpreted in terms of global and local feature processing.

Figure 3

Learning rates for each of the three discrimination pairs in each of the three control (CN) animals. Each data point shows the percent correct on that particular discrimination during each testing session (day). Performance on the congruent discrimination is indicated by the letter “C” and dashed lines. The letter “I” and solid lines indicate performance on the incongruent discrimination, and the letter “R” and dotted lines indicate performance on the random discrimination. For the sake of clarity, data from a specific discrimination pair are not shown after criterion (two consecutive days of ≥90% correct) was reached for that pair.

Figure 4

Learning rates for each of the three discrimination pairs (congruent, incongruent, and random) for each of the three experimental animals (SC) during bilateral deactivation of the superior colliculi. For conventions, see Fig. 3.

Figure 5

The mean number of errors to criterion for each of the three discrimination classes (congruent, incongruent, and random) for the three control (CN) cats and the three animals that that the superior colliculus (SC) deactivated during concurrent learning of the three discriminations. Student's t tests were used to compare the control group with the SC deactivation group. Error bars indicate one SEM.