Cognitive differences in horses performing locomotor versus oral stereotypic behaviour

• Behavioural probes were used as indirect measures of striatal function for stereotypy performing horses.
• Crib-biting horses exhibit evidence of enhanced ventral but decreased dorsal striatal activity.
• Weaving animals show accelerated learning, perhaps due to enhanced ventral striatal activity.
• Crib-biting horses are prone to habitual responding whilst weaving animals are not.
• Crib-biting horses may be at increased risk of overtraining.

Preliminary investigations reveal altered learning patterns in horses performing oral stereotypic behaviour which coincide with differential functioning of the basal ganglia group of brain structures. However, no studies to date have investigated similar differences in the equine locomotor stereotypy phenotype. The aim of this investigation was to employ behavioural probes shown previously to reveal basal ganglia dysfunction to initialise the neurologic studies of locomotor stereotypy and to compare cognitive and neural aspects of the locomotor and oral stereotypy phenotype.Spontaneous blink rate (SBR—number of full left eye-ball occlusions by the eye-lid in 30 min) and behavioural initiation rate (BIR- Behavioural transitions in 30 min) were conducted utilising a sample of crib-biting (n = 8), weaving (n = 8) and stereotypy free (n = 8) animals. Horses were observed within their home box for SBR and BIR, with this being repeated three times over three consecutive days. All horses then completed an extinction learning paradigm featuring sensory specific satiety to dissect appetitive and habitual response patterns. Animals were initially shaped to press an A4 sized conditioned stimulus (CS) card mounted on an operant device for a food reward (5 g pelleted feed). The extinction schedule was then split into two separate tasks. Task 1 required animals to conduct 20 operant responses (OR) followed by sensory devaluation (1 kg freely available feed), whilst Task 2 required 40 OR prior to the devaluation phase. Following reward devaluation horses were subjected to an extinction phase where responses to the CS card were not rewarded.Crib-biting horses demonstrated significantly lower SBR than control (p < 0.05) and weaving (p < 0.01) animals, though BIR was significantly increased for crib-biters (p < 0.01) and weavers (p < 0.05) compared to control equivalents. Both crib-biting and weaving groups acquired the initial operant response significantly faster than controls (p < 0.001) and thus displayed accelerated learning. Moreover, crib-biting horses performed significantly more operant responses during extinction phases 1 and 2 compared to weaving (p < 0.001 and p < 0.01, respectively) and control animals (p < 0.001 and p < 0.001, respectively). Finally, crib-biting horses required significantly more trials to reach total extinction criterion compared to control (p < 0.001) and weaving (p < 0.01) equivalents.These findings agree with previous studies in that crib-biting horses displayed a bias towards habitual response patterns, even in the context of minimal training. This tendency corroborates previous post-mortem evidence of up-regulated ventral and down-regulated dorsomedial activity in the striatum group of brain structures. On the other hand, weaving animals were resistant to over-training and failed to display habitual responding, at any stage of the investigation. This, when taken alongside increased BIR and faster rate of learning is suggestive of enhanced ventral striatal activity but a normal functioning dorsal striatum.