Cognitive appraisal of environmental stimuli induces emotion-like states in fish

Abstract

The occurrence of emotions in non-human animals has been the focus of debate over the years. Recently, an interest in expanding this debate to non-tetrapod vertebrates and to invertebrates has emerged. Within vertebrates, the study of emotion in teleosts is particularly interesting since they represent a divergent evolutionary radiation from that of tetrapods, and thus they provide an insight into the evolution of the biological mechanisms of emotion. We report that Sea Bream exposed to stimuli that vary according to valence (positive, negative) and salience (predictable, unpredictable) exhibit different behavioural, physiological and neuromolecular states. Since according to the dimensional theory of emotion valence and salience define a two-dimensional affective space, our data can be interpreted as evidence for the occurrence of distinctive affective states in fish corresponding to each the four quadrants of the core affective space. Moreover, the fact that the same stimuli presented in a predictable vs. unpredictable way elicited different behavioural, physiological and neuromolecular states, suggests that stimulus appraisal by the individual, rather than an intrinsic characteristic of the stimulus, has triggered the observed responses. Therefore, our data supports the occurrence of emotion-like states in fish that are regulated by the individual's perception of environmental stimuli.

Figure 1

(a,b) Behaviour expressed by fish during the test session (PRDapp = predictable appetitive treatment; UnPRDapp = unpredictable appetitive treatment; PRDavr = predictable aversive treatment; UnPRDavr = unpredictable aversive treatment): (a) frequency of social interactions in the appetitive treatments; (b) frequency of escape attempts in the aversive treatments; (c) plasma cortisol concentrations measured 30 min after the test session (mean ± SEM). Significant differences between treatments (planned comparisons: PRDapp vs. UnPRDapp; PRDavr vs. UnPRDavr; PRDapp vs. PRDavr and UnPRDapp vs. UnPRDavr) are indicated by asterisks (*p < 0.05; **p < 0.01; ***p < 0.001). All descriptive statistics are mean ± SEM.

Figure 2

Expression (mean ± SEM) of the immediate early genes egr-1, c-fos, bdnf and npas4 in the Dm, Dl and Vv brain regions of Sea Bream in the different experimental conditions. Significant differences (planned comparisons) in expression levels between experimental conditions (i.e. PRDapp vs. UnPRDapp; PRDavr vs. UnPRDavr; PRDapp vs. PRDavr and UnPRDapp vs. UnPRDavr) are indicated by asterisks: *p < 0.05; **p < 0.01; ***p < 0.001. All descriptive statistics are mean ± SEM.

Figure 3

Neurogenomic states, as described by correlation (r) matrices of immediate early genes expression in the different brain nuclei (Dm, medial zone of the dorsal telencephalic area; Dl, lateral zone of the dorsal telencephalic area; Vv, ventral nucleus of the ventral telencephalic area) for each affective state (PRDapp = predictable appetitive treatment; UnPRDapp = unpredictable appetitive treatment; PRDavr = predictable aversive treatment; UnPRDavr = unpredictable aversive treatment); Colour scheme represents r-values from -1 (blue) to 1 (red); Asterisks indicate significant correlations after p-value adjustment: *p < 0.05; **p < 0.01; ***p < 0.001; different capital letters indicate significantly different co-expression patterns among affective states, and different small letters indicate significantly different co-expression patterns among brain nuclei, using the QAP correlation test.

Figure 4

Linear discriminant analysis of the four affective states induced by the four experimental treatments (PRDapp = predictable appetitive treatment; UnPRDapp = unpredictable appetitive treatment; PRDavr = predictable aversive treatment; UnPRDavr = unpredictable aversive treatment) as a function of cortisol and immediate early genes levels in all brain regions. Discriminant scores for each individual are plotted.