Emotional and behavioral correlates of mediodorsal thalamic neurons during associative learning in rats - PubMed (original) (raw)

Emotional and behavioral correlates of mediodorsal thalamic neurons during associative learning in rats

T Oyoshi et al. J Neurosci. 1996.

Abstract

Neuronal activity was recorded from the mediodorsal thalamic nucleus (MD) of behaving rats that were trained to lick a protruding spout just after a conditioned stimulus to obtain reward or to avoid shock. Conditioned stimuli included both elemental (auditory or visual stimuli) and configural (simultaneous presentation of auditory and visual stimuli predicting reward outcome opposite that predicted by each stimulus presented alone) stimuli. Of 122 MD neurons responding during the task, the activity of 13 increased just before licking only during the task, but not before spontaneous licking during the intertrial interval (conditioned behavior related). These conditioned behavior-related neurons were located mainly in the lateral MD, which has intimate anatomical connections with motor-related areas such as anterior cingulate and striatum. The activity of the other 109 neurons was related to conditioned stimulation (conditioned stimulus related). Most of these neurons responded differentially to both elemental and configural stimuli in terms of reward contingency, and also changed their responses during extinction and relearning trials. Conditioned stimulus-related neurons with latencies < 300 msec were located mainly in the rostromedial MD, which receives afferents from the basolateral nucleus of the amygdala in which sensory information from various sources converge. Furthermore, most differential neurons that were tested responded during the delay period in a reward task in which a delay was imposed between the conditioned stimulus and reward delivery. The present results, along with previous anatomical studies, suggest the existence of two limbic circuits: anterior cingulate-striatum-lateral MD (motor) and amygdala-medial MD-orbital prefrontal cortex (short-term memory/emotion).

PubMed Disclaimer

Figures

Fig. 1.

Fig. 1.

Experimental diagram. A, Rats were prepared for chronic recording by the formation of receptacles of dental cement to accept artificial earbars. Electrodes were implanted in the ventral tegmental area for ICSS. The rat was trained to lick when the spout was automatically placed close to its mouth. Licking was signaled by a photoelectric sensor triggered by the tongue. Electric shock was delivered from the grid on a floor of a restraining cage.B–D, Time chart of reward task (B), avoidance task (C), and reward task with delay (D). In the reward associative task, one of conditioned sensory stimuli (tone, light, or configural stimuli) associated with and without rewarding stimulus (ICSS or sucrose solution) was presented for 2.0 sec before the spout was placed close to the rat’s mouth (B). In the avoidance task, the rat could avoid electric shock if the spout was licked within 2.0 sec after the conditioned auditory stimulus (C). In the reward task with delay, a conditioned auditory stimulus was presented as in the reward task, but the rat had to wait for a delay period (2.4 sec) before licking a spout. Suc, 0.3

m

sucrose solution.

Fig. 2.

Fig. 2.

Activity of a conditioned behavior-related neuron.A, Activity of a conditioned behavior-related neuron during the reward task. Raw records indicated by a and_b_ show the neuronal and genioglossus EMG activities, respectively. Open and hatched rectangles_at top indicate duration of conditioned stimulus and time of reinforcement, respectively. Each bar below the EMG trace indicates one lick. Neuronal activity increased 35 msec before increase of EMG activity of the genioglossus. B, Activity of a conditioned behavior-related neuron during spontaneous movements of a tongue during intertrial interval. Note that EMG activity increased regardless of the neuronal activity.C, Raster displays and accumulated histogram of the responses of the conditioned behavior-related neuron shown in_A during the reward task. Raster displays and the histogram were aligned with the EMG onset. Each triangle_below a raster line indicates one lick. Time scale in seconds; 0 in time scale indicates onset of the genioglossus EMG activity; each histogram bin, 80 msec. D, Histogram of the mean firing rate for 800 msec before and after the genioglossus EMG onset. Note that the mean firing rate for 800 msec after EMG onset was significantly larger than that before EMG onset (paired_t test; p < 0.05).E, Histogram of the onset times of the 13 conditioned behavior-related neurons preceding that of the genioglossus EMG activity. 0 in time scale; onset of the genioglossus EMG activity. Time scale: seconds.

Fig. 3.

Fig. 3.

Activity of a differential conditioned stimulus-related neuron. A–E, Activity of a differential conditioned stimulus-related neuron during the reward task. A, Response to Tone 1 predicting sucrose solution (Suc); B, response to_Tone 1+Light 1_ predicting no reinforcement;C, response to Light 1 predicting sucrose solution; D, response to Tone 2+Light 2_predicting sucrose solution; E, response to Light 2 predicting no reinforcement. Note that the neuron responded to Tone 1, Light 1, Tone 2+Light 2, and ingestion of sucrose solution, but not to Tone 1+Light 1 or to_Light 2. F, Activity of a differential conditioned stimulus-related neuron during spontaneous movements of the tongue during intertrial interval. Note that activity of the neuron increased regardless of EMG activity in A, C, and_D_ and that EMG activity increased regardless of the neuronal activity in F. Other descriptions as for Figure2.

Fig. 4.

Fig. 4.

Activity of the conditioned stimulus-related neuron shown in Figure 3. A, Raster displays and accumulated histogram of the discharges of the conditioned stimulus-related neuron during the reward task. Raster displays and the histogram were aligned with the EMG onset. Other descriptions as for Figure 2_C_. B, Histogram of the mean firing rates for 800 msec before and after the genioglossus EMG onset. Note no significant difference in neuronal activity before and after onset of the genioglossus EMG activity (paired t test,p > 0.05). Other descriptions as for Figure2_D_.

Fig. 5.

Fig. 5.

Activity of the multimodal differential conditioned stimulus-related neuron shown in Figure 3 during the reward task using auditory conditioned stimuli. A–C, Raster displays and histograms of neuronal responses to Tone 1_predicting sucrose solution (Suc) (A),Tone 3 predicting ICSS(B), and Tone 2 predicting no reinforcement (C). Note that the neuron responded to_Tone 1, Tone 3, and ingestion of sucrose solution, but not to Tone 2. Open and hatched rectangles at top indicate duration of conditioned stimulus and time of reinforcement, respectively. Each_triangle_ below a raster line indicates one lick;top histograms show accumulated neuronal responses, and_bottom histograms_ show accumulated licks. Time scale in seconds; 0 in time scale indicates onset of a conditioned stimulus; minus is pretrial control; each histogram bin, 80 msec.

Fig. 6.

Fig. 6.

Activity of the multimodal differential conditioned stimulus-related neuron shown in Figure 3 during the reward task using visual and configural conditioned stimuli. A, B, Raster displays and histograms of neuronal responses to_Light 1_ predicting sucrose solution (Suc) (Aa), Light 2 predicting no reinforcement (Ab), Tone 2+Light 2 predicting sucrose solution (Ba), and Tone 1+Light 1_predicting no reinforcement (Bb). Note that the neuron responded to Light 1, Tone 2+Light 2, and ingestion of sucrose solution, but not to Light 2 and_Tone 1+Light 1. Other descriptions as for Figure5.

Fig. 7.

Fig. 7.

Activity of a differential conditioned stimulus-related neuron that responded to unimodal (auditory) stimuli.A–C, Raster displays and histograms of neuronal responses to Tone 1 predicting sucrose solution (Suc) (Aa), Tone 3_predicting ICSS (Ab), Tone 2 predicting no reinforcement (Ac), Tone 4 predicting electric shock (Ad),Light 1 predicting sucrose solution (Ba),Light 2 predicting no reinforcement (Bb),Tone 2+Light 2 predicting sucrose solution (Ca), Tone 1+Light 1 predicting no reinforcement (Cb). Note that the neuron responded to conditioned stimuli predicting reward only if the conditioned stimuli included auditory stimulus (i.e., Tone 1, Tone 3, and_Tone 2+Light 2) and that the neuron did not respond to the conditioned visual stimulus predicting reward (Light 1) or other stimuli predicting no reward (Tone 2, Tone 4, Light 2, Tone 1+Light 1). Other descriptions as for Figure5.

Fig. 8.

Fig. 8.

Activity of a nondifferential conditioned stimulus-related neuron that responded indiscriminately to all conditioned sensory stimuli. A–C, Raster displays and histograms of neuronal responses to Tone 1 predicting sucrose solution (Suc) (Aa), Tone 3 predicting ICSS (Ab),Tone 2 predicting no reinforcement (Ac),Tone 4 predicting electric shock (Ad), Light 1 predicting sucrose solution (Ba), Light 2 predicting no reinforcement (Bb), _Tone 2+Light 2_predicting sucrose solution (Ca), Tone 1+Light 1 predicting no reinforcement (Cb). Note that the neuron responded to all conditioned sensory stimuli. Other descriptions as for Figure 5.

Fig. 9.

Fig. 9.

Activity of the differential conditioned stimulus-related neuron shown in Figure 3 during extinction and relearning trials. A, Raster displays of the neuronal discharges during control, extinction, and relearning trials. Trials 1–5, control trials before extinction; trials 6–20, extinction trials; trial 21–35, relearning trials. B, Response magnitude to the conditioned stimulus in each trial (a) and in each block consisting of five trials (b). Response magnitude was defined as the mean firing rate during conditioned sensory stimulation period minus the mean spontaneous firing rate. In Bb, the blocks with_asterisks_ show that the response magnitudes were significantly smaller than that of the control before extinction (Tukey test after one-way ANOVA, p < 0.05). Other descriptions as for Figure 5.

Fig. 10.

Fig. 10.

Activity of a differential conditioned stimulus-related neuron that responded during a delay time in the reward task with delay. A, B, Raster displays and histograms of neuronal responses and the raw records of the genioglossus EMG activity in the reward task without delay (A) and with delay (B). In the reward task with delay, the neuron responded during the delay period (2.4 sec), whereas no EMG activity was observed during the delay period. Other descriptions as for Figure 5.

Fig. 11.

Fig. 11.

Frequency histograms of neuronal response latencies to conditioned sensory stimuli. A, Distributions of neuronal response latencies of unimodal differential conditioned stimulus-related neurons. Top and_bottom histograms_ show the latencies of auditory and visual responsive neurons, respectively. B, Distributions of neuronal response latencies of multimodal differential (top histogram) and nondifferential (bottom histogram) conditioned stimulus-related neurons to auditory (a) and visual (b) conditioned stimuli. Mean latencies of differential conditioned stimulus-related neurons to auditory and visual stimuli were significantly longer than those of nondifferential conditioned stimulus-related neurons (Tukey test after one-way ANOVA, p < 0.05).

Fig. 12.

Fig. 12.

Histograms of mean spontaneous firing rates of differential conditioned stimulus-related, nondifferential conditioned stimulus-related, conditioned behavior-related, and nonresponsive neurons. Asterisks indicate the mean spontaneous firing rates of the nondifferential conditioned stimulus-related neurons, which were significantly higher than those of the others (Tukey test after one-way ANOVA, p < 0.05).

Fig. 13.

Fig. 13.

Locations of the recording sites in the rat MD. Frontal sections, based on the atlas of Paxinos and Watson (1986), are arranged rostrocaudally from left to_right_. Each value below each section indicates distance (mm) posterior from the bregma. Open circles, Responsive neurons; dots, nonresponsive neurons. AD, Anterodorsal thalamic nucleus; CM, central medial thalamic nucleus; CL, centrolateral thalamic nucleus;D3V, dorsal third ventricle; DG, dentate gyrus; fr, fasciculus retroflexus; IMD, intermediodorsal thalamic nucleus; LHb, lateral habenular nucleus; LHbL, lateral habenular nucleus, lateral; LHbM, lateral habenular nucleus, medial;MD, mediodorsal thalamic nucleus; MDC, central segment of mediodorsal thalamic nucleus; MDL, lateral segment of mediodorsal thalamic nucleus; MDM, medial segment of mediodorsal thalamic nucleus; MDPL, paralaminar segment of mediodorsal thalamic nucleus;MHb, medial habenular nucleus; PC, paracentral thalamic nucleus; PF, parafascicular thalamic nucleus; PT, paratenial thalamic nucleus;PV, paraventricular thalamic nucleus;PVA, paraventricular thalamic nucleus, anterior;PVP, paraventricular thalamic nucleus, posterior; PoMn, posteromedian thalamic nucleus.

Fig. 14.

Fig. 14.

Locations of each neuronal type of rat MD neurons. Open triangles, Conditioned behavior-related neurons; solid circles, differential conditioned stimulus-related neurons with short response latencies <300 msec;_open circles_, differential conditioned stimulus-related neurons with long response latencies > 300 msec; open squares, nondifferential conditioned stimulus-related neurons. Other abbreviations as in Figure 13.

References

    1. Aggleton JP, Mishkin M. Visual recognition impairment following medial thalamic lesions in monkeys. Neuropsychologia. 1983;21:189–197. - PubMed
    1. Aggleton JP, Mishkin M. Projection of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol. 1984;222:56–68. - PubMed
    1. Andersen E. Periaqueductal gray and cerebral cortex modulate responses of medial thalamic neurons to noxious stimulation. Brain Res. 1986;375:30–36. - PubMed
    1. Bachevalier J, Mishkin M. Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkey. Behav Brain Res. 1986;20:249–261. - PubMed
    1. Butter CM, Snyder DR. Alternations in aversive and aggressive behaviors following orbital frontal lesions in rhesus monkeys. Acta Neurobiol Exp. 1972;32:525–565. - PubMed

Publication types

MeSH terms

LinkOut - more resources