Social and Ecological Regulation of a Decision-Making Circuit

Abstract

Ecological context, sensory inputs, and the internal physiological state are all factors that need to be integrated for an animal to make appropriate behavioral decisions. However, these factors have rarely been studied in the same system. In the African cichlid fish Astatotilapia burtoni, males alternate between two phenotypes based on position in a social hierarchy. When dominant (DOM), fish display bright body coloration and a wealth of aggressive and reproductive behavioral patterns that make them conspicuous to predators. Subordinate (SUB) males, on the other hand, decrease predation risk by adopting cryptic coloration and schooling behavior. We therefore hypothesized that DOMs would show enhanced startle-escape responsiveness to compensate for their increased predation risk. Indeed, behavioral responses to sound clicks of various intensities showed a significantly higher mean startle rate in DOMs compared with SUBs. Electrophysiological recordings from the Mauthner cells (M-cells), the neurons triggering startle, were performed in anesthetized animals and showed larger synaptic responses to sound clicks in DOMs, consistent with the behavioral results. In addition, the inhibitory drive mediated by interneurons (passive hyperpolarizing potential [PHP] cells) presynaptic to the M-cell was significantly reduced in DOMs. Taken together, the results suggest that the likelihood for an escape to occur for a given auditory stimulus is higher in DOMs because of a more excitable M-cell. More broadly, this study provides an integrative explanation of an ecological and social trade-off at the level of an identifiable decision-making neural circuit.

In Vivo Ca2+ Imaging Reveals that Decreased Dendritic Excitability Drives Startle Habituation

“…Excitatory spiral fiber (SF) neurons, recently implicated in regulating M-cell firing and startle probablility (Lacoste et al, 2015) can likely be excluded on similar grounds as their input lies downstream of the M-cell soma. FF neurons, on the other hand, receive glutamatergic input from VIII afferents and are known to regulate the startle threshold in adult goldfish (Weiss et al, 2008) and African cichlid fish (Neumeister et al, 2010), and in larval zebrafish these neurons are adjacent to the M-cell lateral dendrite (Koyama et al, 2011) where their input likely influences dendritic responses. Our data are consistent with work in adult goldfish showing that inhibitory synapses on the M-cell are potentiated by repeated stimulation through a partially NMDA receptor-dependent pathway (Korn et al, 1992; Oda et al, 1998).…”

Neural Circuit Reconfiguration by Social Status

“…For example, the excitabilities of the Mauthner neuron in fish and the startle response that the neuron triggers both depend on the social status of the animal (Neumeister et al, 2010). Status-dependent circuit reconfiguration in other species may result from proximate mechanisms similar to those described in crayfish, including changes in modulatory function, neuronal thresholds, and the gain or sign of synaptic function (Yeh et al, 1996;Krasne et al, 1997;Herberholz et al, 2001).…”

“…Social status affects neurogenesis in rodents (Kozorovitskiy and Gould, 2004) and crayfish (Song et al, 2007), neuronal size in fish (White et al, 2002), brain morphology in wasps (O'Donnell et al, 2007) and naked mole rats (Holmes et al, 2007), and cell receptor populations in crayfish (Spitzer et al, 2005) and fish (Burmeister et al, 2007). Social status also affects the serotonergic neuromodulation of synaptic responses in both crayfish (Yeh et al, 1996(Yeh et al, , 1997 and fish (Whitaker et al, 2011), and the excitability of neural circuits that produce different behaviors (Krasne et al, 1997;Herberholz et al, 2001;Neumeister et al, 2010). It remains unclear, however, how neural circuits are altered to produce status-dependent behavioral responses.…”

Predation risk modifies behaviour by shaping the response of identified brain neurons

“…A similar result has been observed in a cichlid fish where, in comparison to subordinate males, dominant males were found to display higher startle responsiveness and increased excitability of the Mauthner cell circuit that governs this behaviour. In the latter case, the difference in escape was interpreted as a trade-off between the better reproductive opportunities of being a conspicuous dominant individual and the greater predation risk that this condition represented (Neumeister et al, 2010;Whitaker et al, 2011). In both the crayfish and fish studies, however, the behavioural and neuronal differences were observed by manipulating the social status.…”