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. 1999 Mar 1;19(5):1876-84.
doi: 10.1523/JNEUROSCI.19-05-01876.1999.

Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning

G Schoenbaum  1 , A A Chiba, M Gallagher
Affiliations

Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning

G Schoenbaum et al. J Neurosci. .

Abstract

Orbitofrontal cortex (OFC) is part of a network of structures involved in adaptive behavior and decision making. Interconnections between OFC and basolateral amygdala (ABL) may be critical for encoding the motivational significance of stimuli used to guide behavior. Indeed, much research indicates that neurons in OFC and ABL fire selectively to cues based on their associative significance. In the current study recordings were made in each region within a behavioral paradigm that allowed comparison of the development of associative encoding over the course of learning. In each recording session, rats were presented with novel odors that were informative about the outcome of making a response and had to learn to withhold a response after sampling an odor that signaled a negative outcome. In some cases, reversal training was performed in the same session as the initial learning. Ninety-six of the 328 neurons recorded in OFC and 60 of the 229 neurons recorded in ABL exhibited selective activity during evaluation of the odor cues after learning had occurred. A substantial proportion of those neurons in ABL developed selective activity very early in training, and many reversed selectivity rapidly after reversal. In contrast, those neurons in OFC rarely exhibited selective activity during odor evaluation before the rats reached the criterion for learning, and far fewer reversed selectivity after reversal. The findings support a model in which ABL encodes the motivational significance of cues and OFC uses this information in the selection and execution of an appropriate behavioral strategy.

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Figures

Fig. 1.
Fig. 1.
Schematic drawings illustrate the sequence of behaviors in the go, no-go olfactory discrimination task. In this task, a water-deprived rat had to sample an odor presented at a port on each trial (odor sampling) to decide whether to respond (go response) at a nearby fluid well. Responses at both the odor port and the fluid well were registered by interruption of photo beams that detected entry of the rat’s snout into each port. A go response resulted in delivery of a rewarding sucrose solution, after presentation of a “positive” odor, or an aversive quinine solution, after presentation of a “negative” odor. A go response after a negative odor was considered an error and followed by a prolonged intertrial interval (9 vs 4 sec after a correct response). Novel odors were presented in each session; thus the animal had to learn new associations each day. The rat would begin each session by responding on every trial, irrespective of whether a positive or a negative odor was presented. Learning was evident when the rat began to withhold responses (no-go) after sampling of the negative odor to avoid quinine delivery. This shift in the rat’s behavior generally began after 15–30 trials. Stable, highly accurate performance was generally achieved after 60–100 trials, reaching a behavioral criterion defined as 90% accurate performance over a moving block of 20 trials. During postcriterion performance the rat would make very few errors.
Fig. 2.
Fig. 2.
Electrode recording sites. Photomicrographs of histological sections showing the reconstruction of recording sites in representative subjects in OFC (A) and ABL (B). In each photomicrograph, a vertical line represents the dorsoventral range along the electrode track from which neurons were recorded in the case shown. Below each photomicrograph is a drawing that shows the approximate area in which recordings were obtained in each group. The OFC encompasses the orbital regions and agranular insular cortex. Recordings were localized to ventrolateral and lateral orbital regions (VLO/LO) and ventral agranular insular cortex (AIv) in the four rats in the OFC group. Recordings were localized to the basolateral nucleus in three of the rats in the ABL group (pictured in photomicrograph and as BLAn in drawing) and lateral nucleus in the fourth rat (LAn). (Drawings adapted from Swanson, 1992; photomicrographs adapted from Schoenbaum et al., 1998.)
Fig. 3.
Fig. 3.
Selective activity in ABL during odor evaluation.a, Selective activity for an ABL neuron during evaluation of odor 1 (open bars) and odor 2 (closed bars) represented as a percentage of the pretrial baseline firing rate (24.1 spikes/sec). On initial training, this neuron fired more strongly during evaluation of the positive odor (odor 1) during postcriterion (post) performance [F(1,86) = 83.05; p < 0.001], and similar selectivity was present during precriterion (pre) training [F(1,77) = 4.00; p < 0.05]. During reversal training the neuron changed selectivity based on the new contingencies, developing a higher relative firing rate to the odor signaling sucrose availability [F(1,101) = 22.52; p < 0.001]. Please note that although this example shows a neuron with greater activity to the positive odor, the data shown in Table 1indicate that other cells in ABL fired more strongly during evaluation of the negative odor(s). b, Raster displays showing neural activity on 30 representative trials (n = total trials) during evaluation of each odor before and after reversal, presented in the left and right panels, respectively. Neural activity, with spikes shown as black tick marks within the shaded regions, begins with odor onset and is synchronized to odor offset corresponding to withdrawal from the odor port (thin vertical line). Activity is truncated at the go response when a response was made or after 1500 msec in the event of a no-go. Trials in which a no-go occurred are evident in fading of the shaded region at the end of each raster. Precriterion and postcriterion trials are separated by a small empty space in the displays of both the initial training and reversal training. Note that during initial training, the rat begins the session responding on every trial but gradually starts to withhold responses on the negative trials; very few responses were made to negative odors after criterion is achieved. During postcriterion performance, this neuron is strongly selective for the positive odor. This selectivity is also present during precriterion trials; however, the cell does not fire selectively during the initial block of precriterion trials corresponding to the early segment of training (trials preceding the arrows). During reversal training, the selective activity of the neuron rapidly shifts after only a few trials to reflect the new response contingencies. At that point in reversal training, however, the rat continues to respond after sampling of the formerly positive odor that now signals quinine. Thus the reversal of selective activity in the neuron develops before a reliable change in the rat’s behavioral strategy. It is also clear that this selectivity reflects the significance of an odor cue rather than its sensory features. c, Contrast in activity during evaluation of positive and negative odors during the early (open bars) and late (closed bars) segments of precriterion training, during postcriterion performance (gray bars), and during reversal training (striped bars) for the neurons with postcriterion selectivity in ABL (see Materials and Methods). The activity contrast was calculated as the difference in firing rate during the evaluation of positive and negative odors divided by the sum of those rates, yielding values that ranged from -1 to 1. The calculation was referenced to the selectivity established during postcriterion training. Firing activity between the trials was used to calculate a baseline activity contrast of −0.01 (data not shown). The degree of selectivity changed significantly in ABL [F(4,184) = 39.44; p < 0.000001] during training. Post hoc tests revealed that the degree of selectivity differed from baseline in each phase of training except the early segment. Relative to the early segment, the activity contrast increased significantly in the late segment of precriterion training but was not significantly different between the late segment and the postcriterion performance phase. During reversal the selectivity in the ABL population reversed; the negative values in the contrast indicate that the odor that elicited greater firing activity after reversal differed from the odor that was preferred during initial training. This contrast for reversal trials differed significantly from the contrasts for each other phase, including baseline and the early precriterion segment that showed low selectivity.
Fig. 4.
Fig. 4.
Selective activity in OFC during odor evaluation.a, Neural activity during evaluation of odor 1 (open bars) and odor 2 (closed bars) represented as a percentage of the pretrial baseline firing rate (1.35 spikes/sec). This neuron fired more strongly during evaluation of the positive odor (odor 1) during postcriterion (post) training [F(1,83) = 5.31 (5.08);p < 0.05]. That selectivity was not evident during precriterion (pre) training when the rat had not yet adopted a reliable response strategy to reflect the learned significance of the odors. Furthermore, the selectivity disappeared during reversal training. Please note that although this example shows a neuron with greater activity to the positive odor, the data shown in Table 1 indicate that other cells in OFC fired more strongly during evaluation of the negative odor(s). b, Raster displays showing neural activity on 30 representative trials (n = total trials) during evaluation of each odor before and after reversal, presented in the left andright panels, respectively (for details, see Fig. 3). Again note that the rat begins the session responding on every trial but gradually begins to withhold (striped bars) for the neurons with postcriterion selectivity in OFC (forresponses on the negative trials. During the precriterion phase, the rat makes several intermittent no-go responses, but the neuron fires very little during evaluation of either odor. The selective activity of this neuron develops only after a reliable change in the rat’s behavioral strategy; during postcriterion performance, the neuron fires strongly during evaluation of the positive odor (odor 1). After reversal, the activity during odor evaluation is no longer selective either before or after the rat achieves criterion on the reversed discrimination problem.c, Contrast in activity during evaluation of positive and negative odors during the early (open bars) and late (closed bars) segments of precriterion training, during postcriterion performance (gray bars), and during reversal training details, see Materials and Methods and Fig. 3legend). The degree of selectivity changed significantly in OFC [F(4,192) = 10.16; p < 0.000001] during training. Post hoc tests revealed that the degree of selectivity only differed from the baseline of 0.04 (data not shown) during the postcriterion phase of training. In other words, the activity contrast in OFC was not significantly different between the early and late segments of precriterion training, increasing significantly only during the postcriterion performance phase. During reversal training, the activity contrast decreased significantly relative to postcriterion performance, returning to a value not significantly different from baseline or either the early or the late segment of precriterion training.
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