I'll take the low road: the evolutionary underpinnings of visually triggered fear

Abstract

Although there is general agreement that the central nucleus of the amygdala (CeA) is critical for triggering the neuroendocrine response to visual threats, there is uncertainty about the role of subcortical visual pathways in this process. Primates in general appear to depend less on subcortical visual pathways than other mammals. Yet, imaging studies continue to indicate a role for the superior colliculus and pulvinar nucleus in fear activation, despite disconnects in how these brain structures communicate not only with each other but with the amygdala. Studies in fish and amphibians suggest that the neuroendocrine response to visual threats has remained relatively unchanged for hundreds of millions of years, yet there are still significant data gaps with respect to how visual information is relayed to telencephalic areas homologous to the CeA, particularly in fish. In fact ray finned fishes may have evolved an entirely different mechanism for relaying visual information to the telencephalon. In part because they lack a pathway homologous to the lateral geniculate-striate cortex pathway of mammals, amphibians continue to be an excellent model for studying how stress hormones in turn modulate fear activating visual pathways. Glucocorticoids, melanocortin peptides, and CRF all appear to play some role in modulating sensorimotor processing in the optic tectum. These observations, coupled with data showing control of the hypothalamus-pituitary-adrenal axis by the superior colliculus, suggest a fear/stress/anxiety neuroendocrine circuit that begins with first order synapses in subcortical visual pathways. Thus, comparative studies shed light not only on how fear triggering visual pathways came to be, but how hormones released as a result of this activation modulate these pathways.

The nucleus pretectalis principalis: A pretectal structure hidden in the mammalian thalamus

“…In that sense, evidence from experimentation in amphibians demonstrates that lesions in the pretectum of toads generates a behavioral syndrome in which the animal can no longer differentiate between large (predator‐like) and small (prey‐like) moving objects, resulting in the abolishment of avoidance behavior and the erratic protraction of the tongue toward large moving object; an effect attributed to the inhibitory effect of NPY on the tectal activity (Carr, ). In mammals, Gale and Murphy () recently showed that the intrinsic GABA modulation of horizontal interneurons shapes TGC selectivity to the size of moving disks.…”

The Aversive Brain System of Teleosts: Implications for Neuroscience and Biological Psychiatry

“…These different components process distinct afferent inputs and channel 160 them to parallel downstream efferent pathways, responsible for output circuits for fear of predators 161 and fear of pain (Gross and Canteras, 2012). In zebrafish, sensory input to the posterior 162 telencephalon (including Dm) suggest massive olfactory information (e.g., Miyasaka et al, 2014), 163 while visual and auditory stimuli are processed initially in the optic tectum (Northcutt, 1983;Meek, 164 1990); however, the fact that an olfactory stimulus can be associated with a visual stimulus in the 165 Dm (Ruhl et al, 2017;Lal et al, 2018) suggests the participation of a projection from the optic 166 tectum, possibly via the lateral preglomerular nucleus (Carr, 2015). Thus, in zebrafish the Dm also 167 appears to be important for learned fear, but the participation in unconditioned behavior suggests 168 that either subpopulations of the Dm process different stimuli, or that the evolutionary shift towards 169 visual and auditory stimuli in mammals displaced the massive olfactory projections that was found 170 in fish.…”

“…In addition to this "slow" pathways (the "forebrain circuit"), a "quick-and-dirty" pathway 577 for visual aversive stimuli is organized in the optic tectum (the "midbrain circuit") (Carr, 2015). This 578 midbrain circuit is sensitive to stimulus size and critical angle, and switches from approach (small 579 stimuli probably mean "food") to avoidance (large stimuli arriving at a specific angle probably 580 mean "predator strike").…”

“…Moreover, a putative indirect OT-Dm projection, via the lateral preglomerular nucleus, has been 583 proposed in fish as an analogue of the superior colliculus-pulvinar-amygdala pathway of mammals 584 (Carr, 2015). It is expected that visually threatening stimuli activate the first circuit and bypass the 585…”

“…Not only is the isocortex not the main target of sensory thalamic projections in zebrafish, 597 the participation of putative homologues in aversive behavior has not been established (but see Aoki 598 et al, 2013). Indeed, Carr (2015) suggested that a "high road" is absent in fish, which would only 599 possess a "low road". The present review, however, suggest that some granularity in this 600 interpretation is necessary, given that a differentiation between responses mediated by the forebrain 601 and midbrain circuits is possible.…”