The influence of the trait-like tendency to rely on declarative- or procedural- like memory systems on the development of habits and compulsive behaviours in the rat

Convergent evidence supports a multi-systems organisation of long-term memory in mammals, where different types of memory are underpinned by dissociable neural systems which can operate independently of one another. A key distinction in this regard is that between declarative memory and procedural memory, which differ with respect to whether the information that is stored, encoded and retrieved can be represented in a manner that is independent of the animal’s performance. Individual differences in the reliance on the dissociable neural systems that subserve declarative- like versus procedural-like memory have been characterised in the rat in a spatial discrimination task. In a version of the task that is solvable using either a declarative-like, allocentric place or a procedural-like, egocentric response spatial learning strategy, a “direct opposition” probe can reveal which strategy any individual relies on to solve the task. The distinction among declarative and procedural memory parallels, but is not identical to, the distinction among two behaviourally and neurally dissociable instrumental learning processes that are recruited to acquire and perform behaviours under the control of their consequences: goal-directed (action-outcome) actions and stimulus-response habits. The latter, and in particular its excessive rigidity, has been implicated in the development of compulsive behaviours that are a transdiagnostic feature of various neuropsychiatric disorders such as obsessive-compulsive disorder and substance/alcohol use disorders. Theoretical frameworks and some empirical findings suggest a correspondence between declarative memory and goal-directed actions, on the one hand, and procedural memory and stimulus- response habits, on the other. This might, in turn, suggest that an individual's tendency to rely on response versus place memory systems is associated with a greater tendency to develop stimulus-response habits and the ensuing increased vulnerability to develop compulsive behaviours. The purpose of this thesis is to test this hypothesis. The theoretical background of and experimental techniques used in this thesis are detailed in the General Introduction (Chapter 1) and General Methods (Chapter 2) respectively. Chapter 3 describes a preparation for measuring the individual tendency to rely on place versus response memory systems in a spatial discrimination task in male and female rats. Chapter 4 uses this approach to characterise place/response learning tendency in terms of behavioural traits in rats that have been implicated in the development of habits and compulsive behaviours: trait-like anxiety, novelty preference and sign- versus goal-tracking tendency. I show that “place learner” and “response learner” identity can be predicted by the individuals’ novelty place preference, but not their trait-like anxiety nor their sign- versus goal-tracking tendency. In Chapter 5, I investigate whether the individual tendency to rely on place versus response memory systems influences the development of stimulus-response versus action-outcome control over instrumental responding for food in a free-operant task. I demonstrate that, surprisingly, place learners are more likely to develop stimulus-response habits after extensive instrumental conditioning, a relationship that is confined to females. In Chapter 6, I determine whether place/response learning tendency shapes the acquisition and performance of adjunctive drinking, an instrumental coping response to stress or physiological arousal that can become excessive and thereby compulsive in a subset of individuals. I subsequently determined the place/response learning-dependent associative nature of this instrumental coping response. I show that place and response learners are equally likely to develop coping responses and their compulsive manifestations. However, only in response learners does the locus of control over adjunctive drinking devolve to the habit system. Analysis of the transcriptional signatures of neuronal activation and plasticity in rats given the opportunity to adjunctively consume alcohol revealed a selective reduction in neural activity in the anterior insula and its afferent network in place learners. These results, taken together, challenge conventional thought regarding the relationship between declarative and procedural memory systems and the development of habits and compulsive behaviours.

Name dc:type.qualificationname

Doctor of Philosophy (PhD)

Level dc:type.qualificationlevel

Doctoral

Grantor dc:publisher.institution

University of Cambridge

Year dc:date.issued

2025

Author dc:creator

• Innes, Joseph

Advisor dc:contributor.advisor

• Belin, David

• Compulsive behaviours
• Habits
• Memory
• Spatial navigation

Licence

• https://www.repository.cam.ac.uk/bitstreams/cafcdd52-8f21-437d-a36f-6889da9ee5b1/download
• http://purl.org/NET/rdflicense/allrightsreserved

Language dc:language

eng

Author Identifier

0009-0008-6782-3673

OAI identifier oai:identifier

oai:www.repository.cam.ac.uk:1810/399466