Stereotypic route-tracing in experimentally caged songbirds correlates with general behavioural disinhibition

Abstract

Repetitive, unvarying and apparently functionless behaviours called stereotypies are common in caged animals, but the mechanisms of cage stereotypy have remained elusive. We found that stereotypies correlate with a sign of altered brain functioning, the general disinhibition of behaviour, found in stereotyping human patients and animals treated with psychostimulants. We investigated route-tracing stereotypy in blue tits, Parus caeruleus, and marsh tits, P. palustris, caged in a behavioural research laboratory. In experiment 1, stereotypy correlated with disinhibition of responses, shown as persistent responding in extinction learning. In experiment 2a, stereotypy in blue tits correlated with repetitive sequence generation on a 'gambling task' that specifically measures disinhibited striatal functioning in humans and correlates with stereotypy in autistic and schizophrenic patients. In experiment 2b, the behavioural disinhibition correlated with stereotypy also affected food-storing behaviour in marsh tits, in particular their response to cache pilfering. In experiment 3, the sequencing of nonstereotypic home cage behaviour was correlated with stereotypy. Finally, changes in stereotypy induced by environmental enrichment correlated with changes in these measures of altered behavioural control. These results suggest that housing conditions that cause stereotypy thus alter many aspects of the behavioural control of caged subjects, mediated by altered striatal functioning. The implications for understanding cage stereotypies in laboratory, farm and zoo animals, and for laboratory-based behavioural experiments, are discussed. We suggest that improving housing conditions so that cage stereotypies do not develop would enhance the validity of laboratory-based behavioural research.

Recurrent perseveration correlates with abnormal repetitive locomotion in adult mink but is not reduced by environmental enrichment

“…patterning, or non-randomness) within series of responses [23,[60][61][62]. A similar two-choice guessing task [22,63], also known as a "gambling" task, has been adapted for use with laboratory monkeys [64], birds [35,36], and mice [41,43], and we used an analogous task for mink. Subjects chose between two doors (Fig.…”

“…(1) Third-order Markov Model: following Garner and colleagues [35,36,41], we compared the observed frequency of each of 16 possible 4-response sequences (e.g. RLRR or LRRL) to that expected based on each subject's global side bias.…”

“…Direct evidence that the ARB of Non-enriched captive animals reflects changes in corticostriatal function includes: haloperidol, which inhibits dopaminergic action in the nigrostriatal pathway, prevented captivity-induced jumping in bank voles [30]; and compared to Non-enriched and/or stereotypic deer mice, Enrichedreared individuals with negligible jumping/somersaulting showed elevated cytochrome oxidase activity in the motor cortex, striatum, and nucleus accumbens, elevated dendritic spine density in the motor cortex and striatum, and elevated brain-derived neurotrophic factor in the striatum [31][32][33]. Furthermore, behavioural evidence that captive animals' ARBs are part of a suite of changes inducing generalized disinhibition includes positive correlations between perseveration in operant tasks and ARB in a wide variety of captive species [1,[34][35][36][37][38][39][40][41]. This mounting evidence is sufficiently compelling that two of us have advocated abandoning the traditional, purely descriptive definition of ARB, in favour of a mechanistic definition stipulating that ARB is the product of (among other causes) CNS dysfunction [1,3]: an issue we return to in the discussion.…”

“…Most exceptions have focused on "recurrent" perseveration, defined as the inappropriate repetition of an already completed response to a subsequent stimulus [42]. This type of perseveration correlated positively with repetitive locomotion/oral movements in caged birds [35,36], with bar-mouthing in C57BL/6J mice [41], but not in ICR CD-1 mice [43], and with repetitive movement in clinical human patients [22,23]. Other studies have tied "stuckin-set" perseveration, the inappropriate maintenance of a plan or goal, to more complex ARBs like barbering in mice [1,41] and circumscribed interests in autistic humans [23].…”

“…In some instances this is clear: in deer mice, being raised with or without environmental enrichment induces group differences in jumping/somersaulting, perseveration and post-mortem indices of basal ganglia function [31,32,39]; while in African striped mice, wild-caught animals are less perseverative and show less frequent repetitive movements than captive-born individuals [51]. However, in many other instances, results are based on individual differences within similarly housed and treated subjects [34,35,38,39,41]. These individual differences could reflect normal variation, with a mean and variance no different from Enrichedhoused animals.…”