Dynamic cortical lateralization during olfactory discrimination learning

Abstract

Bilateral cortical circuits are not necessarily symmetrical. Asymmetry, or cerebral lateralization, allows functional specialization of bilateral brain regions and has been described in humans for such diverse functions as perception, memory and emotion. There is also evidence for asymmetry in the human olfactory system, although evidence in non-human animal models is lacking. In the present study, we took advantage of the known changes in olfactory cortical local field potentials that occur over the course of odour discrimination training to test for functional asymmetry in piriform cortical activity during learning. Both right and left piriform cortex local field potential activities were recorded. The results obtained demonstrate a robust interhemispheric asymmetry in anterior piriform cortex activity that emerges during specific stages of odour discrimination learning, with a transient bias toward the left hemisphere. This asymmetry is not apparent during error trials. Furthermore, functional connectivity (coherence) between the bilateral anterior piriform cortices is learning- and context-dependent. Steady-state interhemispheric anterior piriform cortex coherence is reduced during the initial stages of learning and then recovers as animals acquire competent performance. The decrease in coherence is seen relative to bilateral coherence expressed in the home cage, which remains stable across conditioning days. Similarly, transient, trial-related interhemispheric coherence increases with task competence. Taken together, the results demonstrate transient asymmetry in piriform cortical function during odour discrimination learning until mastery, suggesting that each piriform cortex may contribute something unique to odour memory.

Figure 1

Acquisition of discrimination between odour mixtures (n = 5) A, performance on the task was divided into four stages for analyses of LFPs, as described in the Methods. B, example of unfiltered LFP recording and filtered LFP data in the theta (3.9–11.7 Hz), and beta (15.6–35.11 Hz) bands from one rat during odour-port sampling and water reward during behaviourally defined Stage 3. Data were recorded simultaneously from left and right aPCX throughout training, as well as during brief periods in the home cage after training. Notably, in this representative example, the left aPCX shows a stronger beta oscillation than the right aPCX during odour sampling.

Figure 2

Changes in oscillatory activity in left and right aPCX during odour-port sampling (1 s post-trial initiation relative to 1 s prior to trial initiation, all trials combined) A, data from animals that successfully acquired the discrimination task. Evoked-beta power is enhanced as performance improves in both left aPCX and right aPCX. In addition, theta power is enhanced in the right aPCX with training. Note that these changes return toward Stage 1 levels with over-training in the left aPCX but remain elevated in the right aPCX (left aPCX, ^##significant difference in evoked beta power between Stage 3 and Stage 1 and between Stage 3 and Stage 4; right hemisphere, ^##significant difference in evoked beta power between Stage 3 and Stage 1, between Stage 4 and Stage 1 and between Stage 3 and Stage 2; **significant difference in evoked theta power between Stage 3 and Stage 1 and between Stage 3 and Stage 2). B, the controls, which were trained in the task but failed to learn, did not show any significant changes in aPCX activity during the course of training.

Figure 3

An example of the fine temporal resolution obtained with multitaper analysis The colour axis indicates the magnitude of the task-related response in relation to baseline periods (see Methods). Oscillatory activity over the course of correct trials in Stage 3, both in right and left aPCX, collapsed across all five animals. Upper and lower confidence intervals (C.I.) (±99%) are also displayed to indicate the stability of the analyses. Subsequent plots had similarly stable confidence intervals and are not shown. Note the difference in colour scales for each plot. The time scale is shown to the bottom left.

Figure 4

Changes in event-related aPCX activity over the course of training The colour axis indicates the magnitude of the task-related response in relation to baseline periods. The left aPCX shows significant enhancement in oscillatory power during correct trials as performance increases, whereas the simultaneously recorded right aPCX does not. For an estimate of variability, see Fig.3. This asymmetrical activity is most prominent at Stage 3. With over-training, the hemispheres become more symmetrical, with robust oscillatory activity in both aPCXs. The timing of activity during trials also shifts with training, with prominent delays in Stage 3. During the error trials, no differences appeared in activation between the left and right aPCX. Note, for Stages 1–3, the colour scale has a maximum of 4, whereas, in Stage 4, the maximum is 8. The time scale is shown to the bottom left.

Figure 5

The mean fold change in beta frequency oscillatory power from baseline across all four training stages extracted from the analyses shown in Fig.4 for pre-trial initiation, odour sampling and decision/reward phases of trials Note the transient asymmetry between left and right aPCX activity during early stages of training and the return to symmetry in Stage 4. This pattern is expressed both during odour sampling and during decision/reward phases of the trials. The standard error of the mean are displayed, although it is too small to be observed.

Figure 6

The change in left/right interhemispheric coherence in aPCX beta oscillations measured across the entire training session was significantly decreased during the initial stages of training compared to coherence in the home cage As animals approached criterion performance (Stage 3), interhemispheric coherence returned to basal levels. An asterisk indicates a significant (P < 0.05) difference between Stage 1 and 2 operant chamber coherence and coherence in all other stages and locations.

Figure 7

Trial-based aPCX interhemispheric coherence spectra Stage 1 and Stage 4 for correct (A) and error (B) trials. There was a significant enhancement in trial-based coherence between Stages 1 and 4, specifically within the beta frequency band. Coherence values approaching 60 Hz are omitted. C, beta frequency band aPCX interhemispheric coherence significantly increased over the course of training, beginning in Stage 3.