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Bernard W Balleine

Publications and source records attributed to Bernard W Balleine.

At least 19 recordsLinked to original sources

Parallel incentive processing: an integrated view of amygdala function.

The amygdala is a heterogeneous structure that has been implicated in a wide variety of functions, most notably in fear conditioning. From this research, an influential serial model of amygdala processes has emerged in which aversive learning is mediated by the amygdala basolateral nucleus whereas performance, in this case of various defensive reflexes, is mediated by the central nucleus. By contrast, recent evidence from appetitive conditioning studies suggests that the basolateral and central nuclei operate in parallel to mediate distinct incentive processes: the basolateral nucleus encodes emotional events with reference to their particular sensory-specific features, whereas the central nucleus encodes their more general motivational or affective significance. Given that there is little if any direct behavioral evidence for the serial model, we suggest that more attention should be given to the claims of the parallel view.

Amygdala↗

Instrumental learning in hyperdopaminergic mice.

In two experiments we investigated the effects of elevated dopaminergic tone on instrumental learning and performance using dopamine transporter knockdown (DAT KD) mice. In Experiment 1, we showed that both DAT KD mice and wild-type controls were similarly sensitive to outcome devaluation induced by sensory specific satiety, indicating normal action-outcome learning in both groups. In Experiment 2, we used a Pavlovian-to-instrumental transfer procedure to assess the potentiation of instrumental responding by Pavlovian conditional stimuli (CS). Although during the Pavlovian training phase the DAT KD mice entered the food magazine more frequently in the absence of the CS, when tested later both groups showed outcome-selective PIT. These results suggest that the elevated dopaminergic tone reduced the selectivity of stimulus control over conditioned behavior, but did not affect instrumental learning.

Animals↗

Motivational control of blocking.

Hungry and thirsty rats lever pressed for food pellets in 1 visual stimulus (V1) and for a saline solution in another stimulus (V2). In a 2nd phase, the rats were made either hungry or thirsty and pressed for a starch solution in 2 stimulus compounds, each containing 1 of the visual cues and an auditory cue, that is, V1A1 and V2A2. On test, rats responded less to A1 than to A2 when hungry but less to A2 than to A1 when thirsty. Two further experiments replicated this selective blocking effect when the rats were both hungry and thirsty during Phase 2 and demonstrated that the magnitude of blocking was comparable to that observed when the reinforcer identity was held constant across the 2 phases.

Animals↗

Stimulus salience and retrospective revaluation.

The effect of conditioning or extinguishing the more salient element of a previously reinforced compound on responding to the less salient element of that compound was assessed in rats. Experiment 1 established that the 2 elements making up an audiovisual compound differed significantly in salience. In Experiment 2A, compound conditioning was followed by either reinforcement or extinction of either the less or more salient element. On test, evidence of retrospective revaluation of the less salient element was found but not of the more salient element. In Experiment 2B, extinction of the more salient element was found to be more effective than its reinforcement in producing retrospective revaluation of the less salient element. The implications of these results are discussed.

Animals↗

Neural bases of food-seeking: affect, arousal and reward in corticostriatolimbic circuits.

Recent studies suggest that there are multiple 'reward' or 'reward-like' systems that control food seeking; evidence points to two distinct learning processes and four modulatory processes that contribute to the performance of food-related instrumental actions. The learning processes subserve the acquisition of goal-directed and habitual actions and involve the dorsomedial and dorsolateral striatum, respectively. Access to food can function both to reinforce habits and as a reward or goal for actions. Encoding and retrieving the value of a goal appears to be mediated by distinct processes that, contrary to the somatic marker hypothesis, do not appear to depend on a common mechanism but on emotional and more abstract evaluative processes, respectively. The anticipation of reward on the basis of environmental events exerts a further modulatory influence on food seeking that can be dissociated from that of reward itself; earning a reward and anticipating a reward appear to be distinct processes and have been doubly dissociated at the level of the nucleus accumbens. Furthermore, the excitatory influence of reward-related cues can be both quite specific, based on the identity of the reward anticipated, or more general based on its motivational significance. The influence of these two processes on instrumental actions has also been doubly dissociated at the level of the amygdala. Although the complexity of food seeking provides a hurdle for the treatment of eating disorders, the suggestion that these apparently disparate determinants are functionally integrated within larger neural systems may provide novel approaches to these problems.

Affect↗

Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning.

Actions become compulsive when they are no longer controlled by their consequences. Compulsivity can be assessed using the omission procedure in which animals are required to withhold a previously reinforced action to earn reward. The current study tested the hypothesis that inactivation of the dorsolateral striatum (DLS), a structure implicated in habitual behavior, can enhance sensitivity to changes in the action-outcome contingency during omission training, thus leading to a reduction in compulsive responding. Over 10 days rats were trained to press a freely available lever for sucrose reward delivered on interval schedules of reinforcement. After learning to press the lever at a stable and high rate, rats in the omission group received a session in which the rewards were now delayed by pressing the lever; i.e. withholding lever pressing resulted in increased access to reward. A control group was yoked to the omission group and received the same number and pattern of reward delivery but without the omission contingency. Half the rats in each group received infusions of vehicle into the DLS prior to this training whereas the remainder received an infusion of the GABA-A receptor agonist muscimol. On the next day, the effect of these treatments was assessed on a probe test in which the tendency of the various groups to press the lever was assessed in extinction and without drug infusion. Rats that received vehicle infusions prior to the omission session showed complete insensitivity to the newly imposed omission contingency. In contrast, rats given the infusion of muscimol selectively reduced lever pressing compared to yoked controls. Thus, extended training with interval schedules resulted in compulsive lever pressing that prevented the learning of the omission contingency, whereas inactivation of the DLS appeared to enhance the rats' sensitivity to this change in the action-outcome contingency.

Analysis of Variance↗

Lesions of medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning.

Several studies have established that pretraining lesions of the medial prefrontal cortex (mPFC) render instrumental actions insensitive to devaluation of the instrumental outcome and degradation of the action-outcome contingency. Nevertheless, it remains to be assessed whether the involvement of the mPFC in goal-directed action is limited to the acquisition or to the expression of the action-outcome association in performance. The current series of experiments investigated this issue by comparing the effects of mPFC lesions made either before or after initial training using sensitivity to outcome devaluation as an assay of goal-directed performance. Whereas pretraining lesions left performance insensitive to outcome devaluation, posttraining lesions spared this effect. To determine whether the effect of mPFC lesions on outcome devaluation was the result of a more fundamental deficit in response selection, experiment 2 assessed the impact of pretraining and posttraining lesions on the ability of the instrumental outcome to selectively reinstate the performance of its associated action after a period of extinction. Although both lesions attenuated the magnitude of instrumental reinstatement generally, they left intact the ability of the instrumental outcome to influence response selection. Experiment 3 investigated the relationship between the outcome-selective devaluation and reinstatement effects and found evidence that these effects are both behaviorally and neurally dissociable at the level of the mPFC. These results indicate that the mPFC is selectively involved in the acquisition, but not the permanent storage or expression, of action-outcome associations in instrumental conditioning.

Animals↗

Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer.

This series of experiments compared the effects of lesions of the basolateral complex (BLA) and the central nucleus (CN) of the amygdala on a number of tests of instrumental learning and performance and particularly on the contribution of these structures to the specific and general forms of pavlovian-instrumental transfer (PIT). In experiment 1, groups of BLA-, CN-, and sham-lesioned rats were first trained to press two levers, each earning a unique food outcome (pellets or sucrose), after which they were given training in which two auditory stimuli (tone and white noise) were paired with these same outcomes. Tests of specific satiety induced outcome devaluation, and tests of PIT revealed that, although the rats in all of the groups performed similarly during both the instrumental and pavlovian acquisition phases, BLA, but not CN, lesions abolished selective sensitivity to a change in the reward value of the instrumental outcome as well as to the selective excitatory effects of reward-related cues in PIT. In experiment 2, we developed a procedure in which both the general motivational and the specific excitatory effects of pavlovian cues could be assessed in the same animal and found that BLA lesions abolished the outcome-specific but spared the general motivational effects of pavlovian cues. In contrast, lesions of CN abolished the general motivational but spared the specific effects of these cues. Together, these results suggest that the BLA mediates outcome-specific incentive processes, whereas CN is involved in controlling the general motivational influence of reward-related events.

Amygdala↗

Consolidation and reconsolidation of incentive learning in the amygdala.

Incentive learning is the process via which animals update changes in the value of rewards. Current evidence suggests that, for food rewards in rats, this learning process involves the amygdala. However, it remains unclear whether this learning undergoes protein synthesis-dependent consolidation and "reconsolidation" processes in the lateral and basal nuclei of amygdala. Accordingly, we examined this hypothesis by local infusion of protein-synthesis inhibitor after devaluation of a food reward induced by a shift from a food-deprived to a food-sated state in an instrumental conditioning paradigm. Our results show that intra-amygdala infusions of anisomycin, whether given after the initial devaluation or after a second devaluation session, abolished the changes in the value of the food reward produced by incentive learning. This study provides direct evidence that instrumental incentive learning depends on protein synthesis within the amygdala for both consolidation and reconsolidation and extends the demonstrations of protein synthesis-dependent reconsolidation to reward-related memories.

Amygdala↗

Motivational control of second-order conditioning.

Two experiments examined the motivational specificity of the associations that support 2nd-order conditioning. In the 1st phase of each experiment rats were exposed to 2 visual conditioned stimuli (CSs) paired with either a saline or food pellet unconditioned stimulus (US) prior to exposure to 2nd-order conditioning using 2 auditory CSs, 1 paired with each visual CS. Rats' motivational state was then shifted prior to a test such that if and only if specific motivational features of the 1st-order training US played a role in the 2nd-order associative structure would responding to the 2nd-order cues shift appropriately with the state change. Even when the US was irrelevant to the training motivational state, shifts in state revealed that it was encoded within the associative structure supporting 2nd-order responding.

Analysis of Variance↗

Perceptual learning enhances retrospective revaluation of conditioned flavor preferences in rats.

Forward and backward blocking of taste preference learning was compared in rats. In the forward condition, thirsty rats were exposed to a flavor (A) in sucrose solution (+) or in water (-), after which they were exposed to A in compound with another flavor (B) in sucrose solution (i.e., AB+). In the backward condition, these phases were reversed. Consumption of B alone was assessed when rats were food deprived. In the forward condition, rats given A+ consumed less B than rats given A-, providing evidence of forward blocking, whereas in the backward condition, rats given A+ drank more of B than those given A-. Subsequent experiments found that alternating but not blocked preexposure to A and B, when given prior to training, produced blocking of B whether A+ was given before or after AB+, suggesting that prior failures to observe backward blocking reflect failures of discrimination.

Analysis of Variance↗

The role of the dorsomedial striatum in instrumental conditioning.

Considerable evidence suggests that, in instrumental conditioning, rats learn the relationship between actions and their specific consequences or outcomes. The present study examined the role of the dorsomedial striatum (DMS) in this type of learning after excitotoxic lesions and reversible, muscimol-induced inactivation. In three experiments, rats were first trained to press two levers for distinct outcomes, and then tested after training using a variety of behavioural assays that have been established to detect action-outcome learning. In Experiment 1, pre-training lesions of the posterior DMS abolished the sensitivity of rats' instrumental performance to both outcome devaluation and contingency degradation when tested in extinction, whereas lesions of the anterior DMS had no effect. In Experiment 2, both pre-training and post-training lesions of the posterior DMS were equally effective in reducing the sensitivity of performance both to devaluation and degradation treatments. In Experiment 3, the infusion of muscimol into the posterior DMS selectively abolished sensitivity of performance to devaluation and contingency degradation without impairing the ability of rats to discriminate either the instrumental actions performed or the identity of the earned outcomes. Taken together, these results suggest that the posterior region of the DMS is a crucial neural substrate for the acquisition and expression of action-outcome associations in instrumental conditioning.

Animals↗

Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning.

Although there is consensus that instrumental conditioning depends on the encoding of action-outcome associations, it is not known where this learning process is localized in the brain. Recent research suggests that the posterior dorsomedial striatum (pDMS) may be the critical locus of these associations. We tested this hypothesis by examining the contribution of N-methyl-D-aspartate receptors (NMDARs) in the pDMS to action-outcome learning. Rats with bilateral cannulae in the pDMS were first trained to perform two actions (left and right lever presses), for sucrose solution. After the pre-training phase, they were given an infusion of the NMDA antagonist 2-amino-5-phosphonopentanoic acid (APV, 1 mg/mL) or artificial cerebral spinal fluid (ACSF) before a 30-min session in which pressing one lever delivered food pellets and pressing the other delivered fruit punch. Learning during this session was tested the next day by sating the animals on either the pellets or fruit punch before assessing their performance on the two levers in extinction. The ACSF group selectively reduced responding on the lever that, in training, had earned the now devalued outcome, whereas the APV group did not. Experiment 2 replicated the effect of APV during the critical training session but found no effect of APV given after acquisition and before test. Furthermore, Experiment 3 showed that the effect of APV on instrumental learning was restricted to the pDMS; infusion into the dorsolateral striatum did not prevent learning. These experiments provide the first direct evidence that, in instrumental conditioning, NMDARs in the dorsomedial striatum are involved in encoding action-outcome associations.

2-Amino-5-phosphonovalerate↗

The role of Pavlovian cues in alcohol seeking in dependent and nondependent rats.

OBJECTIVE: Recent treatment approaches to substance use disorders have focused on reducing drug use by modifying drug-seeking behaviors in response to drug-associated cues. Understanding the effect of alcohol-related stimuli on alcohol-seeking responses is therefore of interest in the study of alcoholism. The present study examined the impact of ethanol- (ETOH) associated cues on selective ETOH-seeking behavior, using a Pavlovian-instrumental transfer design in groups of alcohol-dependent and nondependent rats. METHOD: Rats (N = 24) received Pavlovian conditioning in which each of two stimuli, a tone and white noise, was paired alternately with a 10% sweetened ETOH solution and a polycose-quinine solution. The rats were trained to perform two instrumental actions, with one action earning access to the sweetened ETOH and the other to the polycose-quinine. After training, half of the animals were made ETOH-dependent by intragastric administration of 36 g/kg of ETOH over 4 days, whereas the remainder received intragastric administration of an isocaloric polycose solution. On the following day, subjects were given a choice extinction test in which they were free to choose between both actions with no outcomes being delivered. During this test, the ETOH- and polycose-associated Pavlovian cues were presented to assess performance of the two instrumental actions both in the presence and absence of these stimuli. RESULTS: Pavlovian cues associated with both the ETOH or the polycose exerted a nonspecific excitatory influence on reward-seeking behavior in both nondependent and alcohol-dependent rats. CONCLUSIONS: Responses through which rats gain access to ETOH appear to be subject to the general excitatory influence of the general motivational arousal induced by reward-related cues. It appears the rats' performance did not depend on encoding the specific consequences of their actions and thus was not affected by the selective retrieval or priming of those consequences in memory.

Alcoholism↗

Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning.

Habits are controlled by antecedent stimuli rather than by goal expectancy. Interval schedules of feedback have been shown to generate habits, as revealed by the insensitivity of behaviour acquired under this schedule to outcome devaluation treatments. Two experiments were conducted to assess the role of the dorsolateral striatum in habit learning. In Experiment 1, sham operated controls and rats with dorsolateral striatum lesions were trained to press a lever for sucrose under interval schedules. After training, the sucrose was devalued by inducing taste aversion to it using lithium chloride, whereas saline injections were given to the controls. Only rats given the devaluation treatment reduced their consumption of sucrose and this reduction was similar in both the sham and the lesioned groups. All rats were then returned to the instrumental chamber for an extinction test, in which the lever was extended but no sucrose was delivered. In contrast to sham operated controls, rats with dorsolateral striatum lesions refrained from pressing the lever if the outcome was devalued. To assess the specificity of the role of dorsolateral striatum in this effect a second experiment was conducted in which a group with lesions of dorsomedial striatum was added. In relation now to both the sham and the dorsomedial lesioned groups, only rats with lesions of dorsolateral striatum significantly reduced responding after outcome devaluation. In conclusion, this study provides direct evidence that the dorsolateral striatum is necessary for habit formation. Furthermore, it suggests that, when the habit system is disrupted, control over instrumental performance reverts to the system controlling the performance of goal-directed instrumental actions.

Animals↗

The role of prelimbic cortex in instrumental conditioning.

Numerous studies have implicated human and primate prefrontal cortex in the ability to hold and manipulate goal or outcome-related information in working memory to guide the performance of forthcoming actions. Here we report that cell-body lesions of prelimbic cortex impair the ability of rats to select an action based on previously encoded action-outcome associations. Rats were food deprived and trained to press two levers, one delivering food pellets and the other a sucrose solution. All rats acquired the lever-press response although the initial acquisition in the prelimbic rats was significantly slower than in sham controls. Furthermore, whereas in sham-lesioned rats, post-training devaluation of one of the two outcomes using a specific satiety procedure produced a selective reduction in performance on the lever that in training delivered the prefed outcome, prelimbic rats failed to show a selective devaluation effect and appeared to reduce performance on both levers non-selectively. Importantly, this impairment only emerged in extinction; in subsequent experiments it was found that, when a specific action-outcome association was cued either by presentation of the outcome itself or by presenting a stimulus previously paired with the outcome, rats demonstrated an ability to select the associated action. These results suggest that action-outcome encoding may be intact in prelimbic rats and that the lesion impaired their ability to retain this learning in working memory in order to establish a course of action. Alternatively, the lesion may have altered the relative contribution of action-outcome and outcome-action associations to instrumental performance. On this account, prelimbic lesions affect action-outcome encoding but leave outcome-action associations intact providing the basis for outcome-mediated initiation of an action sufficient, perhaps, to support acquisition and performance in the lesioned rats.

Animals↗

The effect of lesions of the basolateral amygdala on instrumental conditioning.

In three experiments, we assessed the effect of lesions of the amygdala basolateral complex (BLA) on instrumental conditioning in rats. In experiment 1, the lesion had no effect on the acquisition of either lever pressing or chain pulling in food-deprived rats whether these actions earned food pellets or a maltodextrin solution. The lesion did attenuate, however, the impact of outcome devaluation, induced by sensory-specific satiety, on instrumental performance both when assessed in extinction and when reward was delivered contingent on instrumental performance. In experiment 2, evidence was found to suggest that the lesioned rats differed from shams in their ability to encode the specific action-outcome contingencies to which they were exposed during training: lesioned rats failed to adjust their performance appropriately when the action-outcome contingency was degraded. These effects were not caused by an inability of BLA lesioned rats to discriminate the two instrumental actions; these rats were similar to shams in their acquisition of a heterogeneous instrumental chain involving lever pressing and chain pulling (experiment 3). In experiment 4, however, lesions of the BLA were found to produce a deficit in the ability of rats to use the specific properties of the instrumental outcomes used in the previous experiments to discriminate rewarded from unrewarded actions in a free operant discrimination situation. Together these results suggest that in instrumental conditioning, the BLA mediates outcome encoding, specifically relating the sensory features of nutritive commodities to the emotional consequences induced by their consumption.

Amygdala↗

The L-type calcium channel blocker nimodipine mitigates "learned helplessness" in rats.

We assessed the effect of nimodipine, an L-type calcium channel blocker, on the escape deficit induced by prior exposure to inescapable shock in rats in four experiments. In Experiment 1, we injected rats at each of three time points (i.e., before shock exposure, after shock exposure, and before shuttle escape testing) with one of four doses of nimodipine (0, 0.5, 2.5, 5.0 mg/kg). The 5.0-mg/kg dose was most effective, acting to reduce shuttle escape latencies of inescapably shocked rats to a level comparable with nonshocked controls. No benefit occurred in Experiment 2, however, when nimodipine was administered at only one of the three time points used in the first experiment. Moreover, escape performance did not improve when rats received injections of nimodipine on the 2 days prior the experiment, and then one additional injection at one of the three time points identified above in Experiment 3. Finally, administration of nimodipine at two of the three time points did improve escape responding, but only when injected immediately prior both to shock exposure and the shuttle escape test.

Animals↗