Putative lateral inhibition in sensory processing for directional turns

Abstract

Yafremava LS, Gillette R. Putative lateral inhibition in sensory processing for directional turns. J Neurophysiol 105: 2885-2890, 2011. First published April 13, 2011 doi:10.1152/jn.00124.2011Computing targeted responses is a general problem in goal-directed behaviors. We sought the sensory template for directional turning in the predatory sea slug Pleurobranchaea californica, which calculates precise turn angles by averaging multiple stimulus sites on its chemotactile oral veil (Yafremava LS, Anthony CW, Lane L, Campbell JK, Gillette R. J Exp Biol 210: [561][562][563][564][565][566][567][568][569] 2007). Spiking responses to appetitive chemotactile stimulation were recorded in the two bilateral pairs of oral veil nerves, the large oral veil nerve (LOVN) and the tentacle nerve (TN). The integrative abilities of the peripheral nervous system were significant. Nerve spiking responses to punctate, one-site stimulation of the oral veil followed sigmoid relations as stimuli moved between lateral tentacle and the midline. Receptive fields of LOVN and TN were unilateral, overlapping, and oppositely weighted for responsiveness across the length of oral veil. Simultaneous twosite stimulation caused responses of amplitudes markedly smaller than the sum of corresponding one-site responses. Plots of two-site nerve responses against the summed approximate distances from midline of each site were markedly linear. Thus the sensory paths in the peripheral nervous system show reciprocal occlusion similar to lateral inhibition. This outcome suggests a novel neural function for lateral inhibitory mechanisms, distinct from simple contrast enhancement, in computation of both sensory maps and targeted motor actions.

Implementing Goal-Directed Foraging Decisions of a Simpler Nervous System in Simulation

“…Sensory inputs here are of four kinds: (1) a resource odor signal predicting nutritional content to Pleurobranchaea , the amino acid betaine (Gillette et al, 2000); (2) a specific odor signature for a particular prey species (Noboa and Gillette, 2013); and (3) a place code for the averaged site of sensory input to the sensors (Yafremava et al, 2007; Yafremava and Gillette, 2011). (1) and (2) are summed as Incentive for resource and learned positive and negative values of prey odors (R + and R - , respectively), which is then integrated with motivation (satiation) as appetitive state in the feeding network.…”

“…Bilaterally paired, anterior odor sensors simplify the real animal’s chemotactile oral veil’s function in prey tracking (Yafremava and Gillette, 2011) to report the strengths of odors for betaine, a predictor of nutritional value, and the prey signature odors for Hermissenda and Flabellina . The sensors also transform sensory input into a virtual place code, giving the estimated direction of the source of the strongest odor, on which motor response is patterned.…”

“…Stimulus mapping is analogous to that done in the peripheral nervous system of the animal’s oral veil (Yafremava and Gillette, 2011): a virtual place code represents the averaged location of an odor stimulus as Somatic_Map , and incorporates an analog of lateral inhibition as seen in the animal (Eq. 3.1).…”

A role for dopamine in the peripheral sensory processing of a gastropod mollusc

“…Stimulation before and after sulpiride treatment along the oral veil and tentacles was performed with glass Pasteur pipettes with fire-polished tips (3–5 mm diameter). Pipettes were positioned 1–2 cm in front of the targeted OVTC locus and then gradually extended to contact and gently rub the target site for 2 s. Interstimulus intervals were 30 s. Stimuli were applied at either of two loci along the OVTC, corresponding to the most sensitive regions for the two nerves: for the LOVN, this was 5–10 mm ipsilateral to the OVTC midline, and for the TN, the ipsilateral tentacle [28]. 3–6 stimulations at each site were employed before and at 5 and 60 minutes after sulpiride application.…”

“…The peripheral localization and proposed sensory functions of DA in the soft-bodied gastropods are quite unusual relative to its central localization and functions in the skeletonized arthropods, annelids, and vertebrates. We were prompted to investigate the peripheral sensory-motor network of the predatory sea-slug Pleurobranchaea californica based on the observations that the predator learns to avoid specific prey odor associated with noxious prey defenses [27] and that considerable sensory computations are being carried out before transmission of chemotactile information to the central nervous system (CNS) [28]. We have documented, compared, and extended the findings of DA localization in gastropods to Pleurobranchaea by localization of tyrosine hydroxylase-like immunoreactivity (THli), based on the rate-limiting enzyme in the DA biosynthetic pathway.…”