Neural manifolds for odor-driven innate and acquired appetitive preferences

Abstract

Sensory stimuli evoke spiking neural responses that innately or after learning drive suitable behavioral outputs. How are these spiking activities intrinsically patterned to encode for innate preferences, and could the neural response organization impose constraints on learning? We examined this issue in the locust olfactory system. Using a diverse odor panel, we found that ensemble activities both during (‘ON response’) and after stimulus presentations (‘OFF response’) could be linearly mapped onto overall appetitive preference indices. Although diverse, ON and OFF response patterns generated by innately appetitive odorants were still limited to a low-dimensional subspace (a ‘neural manifold’). Similarly, innately non-appetitive odorants evoked responses that were separable yet confined to another neural manifold. Notably, only odorants that evoked neural response excursions in the appetitive manifold were conducive for learning. In sum, these results provide insights on how encoding for innate preferences can also set limits on associative learning.

Conserved neural dynamics and computations across species in olfaction

“…Additionally, locust behavioral experiments are also beginning to reveal how the spatiotemporal structure of odor responses relate to perception of odor features like valence. Specifically, a recent study used behavioral experiments in locust to demonstrate that population odor response trajectories for different odors clustered according to the innate and even learned valences of the odors 46 . While these data suggest that OFF responses are behaviorally meaningful, future work will be required to determine precisely how odor .…”

“…Suggesting how odor OFF responses may influence behavior, it has been shown that OFF responses in locusts correspond to a behavioral measure of "unsensing" 27 . Additionally, a recent study used behavioral experiments in locust to demonstrate that population odor response trajectories for different odors cluster according to innate and learned valences of odors, indicating that population response structure is related to high-level features of odor perception 45 . While these data suggest that OFF responses are behaviorally meaningful in locusts, no evidence currently exists to suggest how odor OFF responses impact mouse olfactory perception.…”

Modelling low-dimensional interacting brain networks reveals organising principle in human cognition

“…Examples include the representation of movement parameters in the motor cortex 26 , the mapping of spatio-temporal coordinates to the hippocampal cortex during navigation 30 , and the encoding of sensory (e.g. visual 27 , olfactory 28 ) information. While these manifolds can change in response to learning 51 , they are generally stable 52 , and it is believed that they relate to the network of synaptic connections and their strengths; however, the relationship between manifolds and structural features remains difficult to demonstrate 53 .…”

Serotonergic amplification of odor-evoked neural responses maps onto flexible behavioral outcomes

“…In this assay, starved locusts opened their sensory appendages close to the mouth, called maxillary palps, when encountering certain food-related odorants. [25][26][27][28] We examined the palp-opening responses (POR) for an odor panel including four odorants: hexanol (HEX), benzaldehyde (BZA), linalool (LOOL), and ammonium (AMN). Note that hexanol (green) is a green-leaf volatile 29 , and benzaldehyde (blue) is a putative locust aggregation pheromone 30 .…”

“…The odor stimulus was delivered using a standard procedure. 26,28,[41][42][43] Briefly, all odorants were diluted to their 0.01-10% concentration by volume (v/v) in mineral oil. Ammonium alone was diluted in distilled water.…”