Effects of degree and timing of social housing on reversal learning and response to novel objects in dairy calves

Rodents and primates deprived of early social contact exhibit deficits in learning and behavioural flexibility. They often also exhibit apparent signs of elevated anxiety, although the relationship between these effects has not been studied. To investigate whether dairy calves are similarly affected, we first compared calves housed in standard individual pens (n = 7) to those housed in a dynamic group with access to their mothers (n = 8). All calves learned to approach the correct stimulus in a visual discrimination task. Only one individually housed calf was able to re-learn the task when the stimuli were reversed, compared to all but one calf from the group. A second experiment investigated whether this effect might be explained by anxiety in individually housed animals interfering with their learning, and tested varying degrees of social contact in addition to the complex group: pair housing beginning early (approximately 6 days old) and late (6 weeks old). Again, fewer individually reared calves learned the reversal task (2 of 10 or 20%) compared to early paired and grouped calves (16 of 21 or 76% of calves). Late paired calves had intermediate success. Individually housed calves were slower to touch novel objects, but the magnitude of the fear response did not correlate with reversal performance. We conclude that individually housed calves have learning deficits, but these deficits were not likely associated with increased anxiety

Calf approach responses in the cognitive bias task

Calf approach responses to each screen for each session before and after disbudding (%). Approach responses have been averaged across trials (23 each of positive and negative screens; 5 of each ambigous screen) within each sessio

Data from: Pain and pessimism: dairy calves exhibit negative judgement bias following hot-iron disbudding

Pain is defined as an unpleasant sensory and emotional experience associated with actual or potential tissue damage, but emotional states are difficult to directly assess in animals. Researchers have assessed pain using behavioural and physiological measures, but these approaches are limited to understanding the arousal rather than valence of the emotional experience. Cognitive bias tasks show that depressed humans judge ambiguous events negatively and this technique has been applied to assess emotional states in animals. However, limited research has examined how pain states affect cognitive processes in animals. Here we present the first evidence of cognitive bias in response to pain in any non-human species. In two experiments, dairy calves (n = 17) were trained to respond differentially to red and white video screens and then tested with unreinforced ambiguous colours in two or three test sessions before and two sessions after the routine practice of hot-iron disbudding. After disbudding calves were more likely to judge ambiguous colours as negative. This ‘pessimistic’ bias indicates that post-operative pain following hot-iron disbudding results in a negative change in emotional state

Mean±SE % GO responses to screens presented during test sessions before and after a) dehorning (n = 12 calves) and b) separation from the dam (n = 8 calves).

<p>Responses are shown separately for the two training screens (positive and negative) and for the three ambiguous probe screens (near-positive, intermediate and near-negative).</p

Pain and Pessimism: Dairy Calves Exhibit Negative Judgement Bias following Hot-Iron Disbudding

<div><p>Pain is defined as an unpleasant sensory and emotional experience associated with actual or potential tissue damage, but emotional states are difficult to directly assess in animals. Researchers have assessed pain using behavioural and physiological measures, but these approaches are limited to understanding the arousal rather than valence of the emotional experience. Cognitive bias tasks show that depressed humans judge ambiguous events negatively and this technique has been applied to assess emotional states in animals. However, limited research has examined how pain states affect cognitive processes in animals. Here we present the first evidence of cognitive bias in response to pain in any non-human species. In two experiments, dairy calves (n = 17) were trained to respond differentially to red and white video screens and then tested with unreinforced ambiguous colours in two or three test sessions before and two sessions after the routine practice of hot-iron disbudding. After disbudding calves were more likely to judge ambiguous colours as negative. This ‘pessimistic’ bias indicates that post-operative pain following hot-iron disbudding results in a negative change in emotional state.</p></div

Mean±SE % GO responses to the three ambiguous probe screens (near-positive, intermediate and near-negative) in multiple sessions before dehorning and before separation from dam and multiple sessions after dehorning and after separation from dam.

<p>Different letter indicate a statistically significant difference (p>0.05).</p

Mean ± SE approach responses of calves to each screen colour before and after disbudding.

<p>Calves were trained to approach the positive screen colour for a milk reward, and to avoid approaching the negative screen colour, and were tested with unreinforced ambiguous colours. Calves responded to the ambiguous colours less frequently after versus before disbudding (<i>p</i> = 0.0004); as expected, there was no effect of disbudding on the responses to positive and negative training colours.</p

Response of calves to anxiety tests at approx. 40–41 d of age.

<p>n = 22 Individual, 13 Early Pair, 9 Group. <b>(a) Latency to touch a novel object was lowest in group-housed calves at approx. 40 d of age</b>. Values are medians with interquartile ranges (maximum value of 10 min assigned to calves who did not make contact). ** indicates a treatment that significantly differs from the others at P<0.05. (<b>b) Latency of calves to touch a familiar human in a handling test was higher in group-housed than in individually housed calves at approximately 41 d of age</b>. Values are means + SE (maximum value of 90 s assigned to calves who did not make contact). Treatments that do not have the same letter differ from each other at P<0.05.</p

Number of sessions taken to reach criterion in the reversal task in Experiment 2.

<p>Values are means + SE (maximum value of 24 assigned to calves who did not learn). Sample sizes as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0132828#pone.0132828.g002" target="_blank">Fig 2</a>. Early social = calves that were pair- or group-housed since early life (Early Pair + Group). * indicates a statistical tendency (0.05</p

Percentage of calves able to reach criterion in the reversal learning task was higher in calves socially housed in early life than in those housed individually in Experiment 2.

<p>** indicates a significant difference at P<0.05. n = 10 individual, 12 late pair, 12 early pair, 9 group.</p