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.

Keywords: amphibian; anxiety; fear; fish; optic tectum; stress; superior colliculus.

Figure 1

The concept of the high road (cortical) and low road (subcortical) visual pathways for processing fear in primates. On the high road, visual information from retinal ganglion cells is relayed to the visual cortex via the lateral geniculate nucleus, a brain area in the thalamus. Visual information is processed through several areas of the cortex before it's sent to the amygdala, whereupon autonomic and endocrine mediators of fear are engaged. On the low road, visual information is sent first to the superior colliculus in the midbrain before being relayed to the amygdala via the pulvinar nucleus. Adapted from Pessoa and Adolphs (2010). LGN, lateral geniculate nucleus; SC, superior colliculus; TE, inferior temporal cortex; TEO, inferior temporal cortex; V, visual cortex.

Figure 2

Organization of subcortical visual pathways triggering fear in humans (A), rodents (B), amphibians (C), and fish (D). Homologous structures are color coded. Putative homologies are represented by dashed lines. ANS, autonomic nervous system; CeA, central amygdala; Dm, medial zone of the dorsal telencephalon; HPA, hypothalamus-pituitary-adrenal axis; HPI, hypothalamus-pituitary-interrenal axis; LP, lateroposterior dorsal thalamic complex; Lpv, lateral posteroventral thalamic nucleus; Mg, magnocellular preoptic nucleus; NPO, nucleus preopticus; OT, optic tectum; P, pulvinar nucleus; PGl, lateral preglomerular nucleus; PVN, paraventricular nucleus; SC, superior colliculus; Vs, supracommisural nucleus of the area ventralis telencephali.

Figure 3

Stress hormones and neuropeptides modulate subcortical visual pathways in anurans. Anurans provide an excellent model for studying how various stress hormones modulate subcortical visual pathway, as the lateral geniculate-striate cortex pathway is absent in amphibians as a group. As shown in this sagittal section of the anuran brain (rostral to the left), corticotropin-releasing factor (CRF) is produced by interneurons in the optic tectum (OT), in addition hypophysiotropic CRF neurons (dashed red line, indicates possible innervation) may project to the retinorecipient layers (layer 9) of the OT. N-acetyl ACTH_1-13 amide (alpha melanocyte-stimulating hormone, α-MSH) neurons in the ventral infundibular nucleus (VIN), homologous to the arcuate nucleus in mammals, also projects to the OT and modulate prey capture. Neuropeptide Y (NPY) produced by neurons in the lateroposterodorsal nucleus (LPd) of the thalamus acts within the OT to reduce approach and prey capture behavior, presumably when a visual threat is present, as this part of the thalamus receives visual information about predators. Corticosterone (CORT) produced by cells in the interrenal glands acts on glucocorticoid receptors in the OT to modulate subcortical visual processing in an as of yet unidentified way. PO, preoptic area; Mg, magnocellular preoptic nucleus; OC, optic chiasm.