Fold Change Detection in Visual Processing

Abstract

Visual processing transforms the complexities of the visual world into useful information. Ciona, an invertebrate chordate and close relative of the vertebrates, has one of the simplest nervous systems known, yet has a range of visuomotor behaviors. This simplicity has facilitated studies linking behavior and neural circuitry. Ciona larvae have two distinct visuomotor behaviors – a looming shadow response and negative phototaxis. These are mediated by separate neural circuits that initiate from different clusters of photoreceptors, with both projecting to a CNS structure called the posterior brain vesicle (pBV). We report here that inputs from both circuits are processed to generate fold change detection (FCD) outputs. In FCD, the behavioral response scales with the relative fold change in input, but is invariant to the overall magnitude of the stimulus. Moreover, the two visuomotor behaviors have fundamentally different stimulus/response relationships – indicative of differing circuit strategies, with the looming shadow response showing a power relationship to fold change, while the navigation behavior responds linearly. Pharmacological modulation of the FCD response points to the FCD circuits lying outside of the visual organ (the ocellus), with the pBV being the most likely location. Consistent with these observations, the connectivity and properties of pBV interneurons conform to known FCD circuit motifs, but with different circuit architectures for the two circuits. The negative phototaxis circuit forms a putative incoherent feedforward loop that involves interconnecting cholinergic and GABAergic interneurons. The looming shadow circuit uses the same cholinergic and GABAergic interneurons, but with different synaptic inputs to create a putative non-linear integral feedback loop. These differing circuit architectures are consistent with the behavioral outputs of the two circuits. Finally, while some reports have highlighted parallels between the pBV and the vertebrate midbrain, suggesting a common origin for the two, others reports have disputed this, suggesting that invertebrate chordates lack a midbrain homolog. The convergence of visual inputs at the pBV, and its putative role in visual processing reported here and in previous publications, lends further support to the proposed common origin of the pBV and the vertebrate midbrain.

A whole nervous system atlas of glutamate receptors reveals distinct receptor roles in sensorimotor circuits

“…In other words, glutamate could serve a modulatory role in the dimming response circuit, perhaps acting via GABA receptors, as has been shown previously (Marsden et al, 2007). Moreover, like the phototaxis behavior, the dimming response shows fold-change detection, although with a different putative circuit motif than in the phototaxis circuit (Borba et al, 2021), and modulation of GABA receptors could serve as the "memory" component of the fold-change detection circuit, as has been described for other systems showing fold-change detection (Lyashenko et al, 2020).…”

“…Namely, AMPA-Rs mediate fast excitatory responses while NMDA-Rs have a slower modulatory role. Moreover, we hypothesized previously that the projection of the PR-I photoreceptors to both excitatory and inhibitory primary interneurons constitute an incoherent feedforward loop circuit motif that functions in visual processing to generate the observed fold-change detection behavior in phototaxis (Borba et al, 2021). In fold-change detection the response scales with the magnitude of the temporal change in sensory input, not with the absolute value of the input (Adler and Alon, 2018).…”

“…Image series were collected using a Hamamatsu Orca-ER camera fitted on a Navitar 7000 macro zoom lens. Programmable 700 and 505 nm LED lamps (Mightex) mounted above the petri dishes were used for dimming response assays as described previously (Borba et al, 2021;Bostwick et al, 2020;Kourakis et al, 2019). The dim response movies were recorded at 10 frames per second (fps).…”

“…At the anatomical level, the Ciona CNS is subdivided into domains showing homology to the vertebrate forebrain, midbrain, hindbrain, midbrain-hindbrain boundary (MHB), and spinal cord (Figure 1a). These homologies are evident in Ciona's developmental mechanisms, gene expression, anatomy, and most recently in neuron classification and synaptic connectivity (Borba et al, 2021;Hudson, 2016;Ryan et al, 2017;Wada et al, 1998). Early descriptions of larval tunicate nervous systems, often made before the above homologies were clear, led to the naming of these anatomical domains with names that do not reflect this homology (e.g., anterior sensory vesicle or anterior brain vesicle for the Ciona forebrain homolog, and visceral or motor ganglion for the hindbrain homolog).…”

Transitions of motor neuron activities during Ciona development

“…Because ascidians are vertebrates' closest relatives (Satoh et al, 2014), they are studied intensively in the fields of chordate evolution and developmental biology. In addition, the cell lineage and neural connectome of Ciona larvae are already revealed (Horie et al, 2008;2009;Ryan et al, 2016;Gibboney et al, 2020;Kim et al, 2020;Borba et al, 2021;Kourakis et al, 2021;Olivo et al, 2021). Their larval neural network consists of only <330 neurons, and their CNS exhibits anatomical asymmetry (Kourakis et al, 2021).…”