Barbara J. Knowlton

A Neostriatal Habit Learning System in Humans

Amnesic patients and nondemented patients with Parkinsons disease were given a probabilistic classification task in which they learned which of two outcomes would occur on each trial, given the particular combination of cues that appeared. Amnesic patients exhibited normal learning of the task but had severely impaired declarative memory for the training episode. In contrast, patients with Parkinsons disease failed to learn the probabilistic classification task, despite having intact memory for the training episode. This double dissociation shows that the limbic-diencephalic regions damaged in amnesia and the neostriatum damaged in Parkinsons disease support separate and parallel learning systems. In humans, the neostriatum (caudate nucleus and putamen) is essential for the gradual, incremental learning of associations that is characteristic of habit learning. The neostriatum is important not just for motor behavior and motor learning but also for acquiring nonmotor dispositions and tendencies that depend on new associations.

The role of the basal ganglia in habit formation

Many organisms, especially humans, are characterized by their capacity for intentional, goal-directed actions. However, similar behaviours often proceed automatically, as habitual responses to antecedent stimuli. How are goal-directed actions transformed into habitual responses? Recent work combining modern behavioural assays and neurobiological analysis of the basal ganglia has begun to yield insights into the neural basis of habit formation.

Remembering episodes: a selective role for the hippocampus during retrieval

Some memories are linked to a specific time and place, allowing one to re-experience the original event, whereas others are accompanied only by a feeling of familiarity. To uncover the distinct neural bases for these two types of memory, we measured brain activity during memory retrieval using event-related functional magnetic resonance imaging. We show that activity in the hippocampus increased only when retrieval was accompanied by conscious recollection of the learning episode. Hippocampal activity did not increase for items recognized based on familiarity or for unrecognized items. These results indicate that the hippocampus selectively supports the retrieval of episodic memories.

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.

The Neural Correlates of Motor Skill Automaticity

Acquisition of a new skill is generally associated with a decrease in the need for effortful control over performance, leading to the development of automaticity. Automaticity by definition has been achieved when performance of a primary task is minimally affected by other ongoing tasks. The neural basis of automaticity was examined by testing subjects in a serial reaction time (SRT) task under both single-task and dual-task conditions. The diminishing cost of dual-task performance was used as an index for automaticity. Subjects performed the SRT task during two functional magnetic imaging sessions separated by 3 h of behavioral training over multiple days. Behavioral data showed that, by the end of testing, subjects had automated performance of the SRT task. Before behavioral training, performance of the SRT task concurrently with the secondary task elicited activation in a wide network of frontal and striatal regions, as well as parietal lobe. After extensive behavioral training, dual-task performance showed comparatively less activity in bilateral ventral premotor regions, right middle frontal gyrus, and right caudate body; activity in other prefrontal and striatal regions decreased equally for single-task and dual-task conditions. These data suggest that lateral and dorsolateral prefrontal regions, and their corresponding striatal targets, subserve the executive processes involved in novice dual-task performance. The results also showed that supplementary motor area and putamen/globus pallidus regions showed training-related decreases for sequence conditions but not for random conditions, confirming the role of these regions in the representation of learned motor sequences.

A System for Relational Reasoning in Human Prefrontal Cortex

The integration of multiple relations between mental representations is critical for higher level cognition. For both deductive- and inductive-reasoning tasks, patients with prefrontal damage exhibited a selective and catastrophic deficit in the integration of relations, whereas patients with anterior temporal lobe damage, matched for overall IQ but with intact prefrontal cortex, exhibited normal relational integration. In contrast, prefrontal patients performed more accurately than temporal patients on tests of both episodic memory and semantic knowledge. These double dissociations suggest that integration of relations is a specific source of cognitive complexity for which intact prefrontal cortex is essential. The integration of relations may be the fundamental common factor linking the diverse abilities that depend on prefrontal function, such as planning, problem solving, and fluid intelligence.

Artificial grammar learning depends on implicit acquisition of both abstract and exemplar-specific information.

The contributions of exemplar-specific and abstract knowledge to artificial grammar learning were examined in amnesic patients and controls. In Experiment 1, grammatical rule adherence and chunk strength exerted separate effects on grammaticality judgments. Amnesic patients exhibited intact classification performance, demonstrating the same pattern of results as controls. In Experiment 2, amnesic patients exhibited impaired declarative memory for chunks. In Experiment 3, both amnesic patients and controls exhibited transfer when tested with a letter set different than the one used for training, although performance was better when the same letter sets were used at training and test. The results suggest that individuals learn both abstract information about training items and exemplar-specific information about chunk strength and that both types of learning occur independently of declarative memory.

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.

Remembering and knowing: two different expressions of declarative memory.

Amnesic patients and a control group were given a recognition test 10 min after studying words. For each recognized word, participants indicated whether they remembered it (R) or whether simply they knew that the word was presented but had no recollections about it (K). The patients were impaired for both R and K responses, performing like a control group tested after 1 week. Another control group was tested both 10 min and 1 week after study. The proportion of words initially eliciting an R response and later eliciting a K response exceeded the proportion of K responses that shifted to R responses. These data are accounted for if items initially eliciting R responses can also elicit K responses. We conclude that the R-K distinction does not reflect the operation of explicit and implicit memory but reflects instead a distinction within declarative memory. Thus, K responses depend on brain structures damaged in amnesia; R responses depend on these same structures and also on the frontal lobes for contextual information.

Intact Artificial Grammar Learning in Amnesia: Dissociation of Classification Learning and Explicit Memory for Specific Instances

The present study investigates whether the ability to classify on the basis of rules can be learned independently of memory for the specific instances used to leach the rules. Thirteen amnesic patients and 14 control subjects studied letter strings generated by an artificial grammar. Subjects were then shown new letter strings and were instructed to classify them as grammatical or nongrammatical. Amnesic patients performed as well as normal subjects. However, amnesic patients performed more poorly than control subjects on a recognition test of the exemplars that had been presented. Amnesic patients also performed more poorly than control subjects when the instructions were to base the classification on explicit comparison with the original exemplars. The results show that classification learning based on exemplars of an artificial grammar can develop normally despite impaired memory for the exemplars themselves. Whereas exemplar memory depends on interactions between neocortex and the limbic system, classification learning may depend on interaction between neocortex and the neostriatum.