The PROUST hypothesis: the embodiment of olfactory cognition

Abstract

The extension of cognition beyond the brain to the body and beyond the body to the environment is an area of debate in philosophy and the cognitive sciences. Yet, these debates largely overlook olfaction, a sensory modality used by most animals. Here, I use the philosopher’s framework to explore the implications of embodiment for olfactory cognition. The philosopher’s 4E framework comprises embodied cognition, emerging from a nervous system characterized by its interactions with its body. The necessity of action for perception adds enacted cognition. Cognition is further embedded in the sensory inputs of the individual and is extended beyond the individual to information stored in its physical and social environments. Further, embodiment must fulfill the criterion of mutual manipulability, where an agent’s cognitive state is involved in continual, reciprocal influences with its environment. Cognition cannot be understood divorced from evolutionary history, however, and I propose adding evolved, as a fifth term to the 4E framework. We must, therefore, begin at the beginning, with chemosensation, a sensory modality that underlies purposive behavior, from bacteria to humans. The PROUST hypothesis (perceiving and reconstructing odor utility in space and time) describers how olfaction, this ancient scaffold and common denominator of animal cognition, fulfills the criteria of embodied cognition. Olfactory cognition, with its near universal taxonomic distribution as well as the near absence of conscious representation in humans, may offer us the best sensorimotor system for the study of embodiment.

Cognitive Mapping and Episodic Memory Emerge From Simple Associative Learning Rules

“…The FAM allows the ASIMOV agent to learn landmark features and rewarding items in its spatial environment, reproducing a potential early phase in the evolution of simpler episodic memory. In particular, the FAM shows how spatial cognitive mapping may have evolved from a simple olfactory learning system, much like how directional olfaction has been hypothesized as the basis for evolution of spatial cognitive mapping and hippocampal-like circuitry [9,10], and furthermore, it shows how autonoetic consciousness may have evolved from systems controlling decision-making in spatial foraging [11,12].…”

A common modular design of nervous systems originating in soft-bodied invertebrates

“…Olfactory bulb, cortex, pallial amygdala, and other pallial structures are thought to have evolved as elaborations of the olfactory system, with the addition of more sensory inputs from complex exteroceptors such as mediate vision, audition, proprioception, and taste ( Reiner et al, 1998 ; Redgrave et al, 1999 ; Smeets et al, 2000 ; Aboitiz et al, 2003 ; Grillner et al, 2013 ; Aboitiz and Montiel, 2015 ; Jacobs, 2023 ). Functionally, these structures interact with each other and the subpallial striatum to integrate reward, motivation, affect, and memory to compute incentive for decision making and to place it in physical context with directional information.…”

“…Elaboration of olfactory systems and associated structures for odor learning is closely tied to the emergence of pallial structures. Directional olfaction may have formed the basis for the evolution of memory organization in the bilaterian brain, with hippocampal-like structures used for mapping and encoding the spatial distributions of novel odorants ( Jacobs, 2012 ; 2023 ). Further, the olfactory system is the only sensory system that bypasses the thalamus, a structure for multi-modal sensory relay; instead, the olfactory bulb projects directly to amygdala and piriform cortex, which are important for emotion and memory ( Kay and Sherman, 2007 ; Jacobs, 2023 ).…”

“…Directional olfaction may have formed the basis for the evolution of memory organization in the bilaterian brain, with hippocampal-like structures used for mapping and encoding the spatial distributions of novel odorants ( Jacobs, 2012 ; 2023 ). Further, the olfactory system is the only sensory system that bypasses the thalamus, a structure for multi-modal sensory relay; instead, the olfactory bulb projects directly to amygdala and piriform cortex, which are important for emotion and memory ( Kay and Sherman, 2007 ; Jacobs, 2023 ). Like the olfactory bulb, the SeN of Pleurobranchaea is notably dopaminergic and is richly innervated by the serotonergic neurons of the C-cluster.…”