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Daily experience suggests that we perceive distances near us linearly. However, the actual geometry of spatial representation in the brain is unknown. Here we report that neurons in the CA1 region of rat hippocampus that mediate spatial perception represent space according to a non-linear hyperbolic geometry. This geometry uses an exponential scale and yields greater positional information than a linear scale. We found that the size of the representation matches the optimal predictions for the number of CA1 neurons. The representations also dynamically expanded proportional to the logarithm of time that the animal spent exploring the environment, in correspondence with the maximal mutual information that can be received. The dynamic changes tracked even small variations due to changes in the running speed of the animal. These results demonstrate how neural circuits achieve efficient representations using dynamic hyperbolic geometry.

 

Using odors to find food and mates is one of the most ancient and highly conserved behaviors. Arthropods from flies to moths to crabs use broadly similar strategies to navigate toward odor sources—such as integrating flow information with odor information, comparing odor concentration across sensors, and integrating odor information over time. Because arthropods share many homologous brain structures—antennal lobes for processing olfactory information, mechanosensors for processing flow, mushroom bodies (or hemi-ellipsoid bodies) for associative learning, and central complexes for navigation, it is likely that these closely related behaviors are mediated by conserved neural circuits. However, differences in the types of odors they seek, the physics of odor dispersal, and the physics of locomotion in water, air, and on substrates mean that these circuits must have adapted to generate a wide diversity of odor-seeking behaviors. In this review, we discuss common strategies and specializations observed in olfactory navigation behavior across arthropods, and review our current knowledge about the neural circuits subserving this behavior. We propose that a comparative study of arthropod nervous systems may provide insight into how a set of basic circuit structures has diversified to generate behavior adapted to different environments.

 

Sensory processing in olfactory systems is organized across olfactory bulb glomeruli, wherein axons of peripheral sensory neurons expressing the same olfactory receptor co-terminate to transmit receptor-specific activity to central neurons. Understanding how receptors map to glomeruli is therefore critical to understanding olfaction. High-throughput spatial transcriptomics is a rapidly advancing field, but low-abundance olfactory receptor expression within glomeruli has previously precluded high-throughput mapping of receptors to glomeruli in the mouse. Here we combined sequential sectioning along the anteroposterior, dorsoventral, and mediolateral axes with target capture enrichment sequencing to overcome low-abundance target expression. This strategy allowed us to spatially map 86% of olfactory receptors across the olfactory bulb and uncover a relationship between OR sequence and glomerular position.

 

To navigate towards a food source, animals frequently combine odor cues about source identity with wind direction cues about source location. Where and how these two cues are integrated to support navigation is unclear. Here we describe a pathway to theDrosophilafan-shaped body that encodes attractive odor and promotes upwind navigation. We show that neurons throughout this pathway encode odor, but not wind direction. Using connectomics, we identify fan-shaped body local neurons called h∆C that receive input from this odor pathway and a previously described wind pathway. We show that h∆C neurons exhibit odor-gated, wind direction-tuned activity, that sparse activation of h∆C neurons promotes navigation in a reproducible direction, and that h∆C activity is required for persistent upwind orientation during odor. Based on connectome data, we develop a computational model showing how h∆C activity can promote navigation towards a goal such as an upwind odor source. Our results suggest that odor and wind cues are processed by separate pathways and integrated within the fan-shaped body to support goal-directed navigation.

 

We consider a common measurement paradigm, where an unknown subset of an affine space is measured by unknown continuous quasi-convex functions. Given the measurement data, can one determine the dimension of this space? In this paper, we develop a method for inferring the intrinsic dimension of the data from measurements by quasi-convex functions, under natural assumptions. The dimension inference problem depends only on discrete data of the ordering of the measured points of space, induced by the sensor functions. We construct a filtration of Dowker complexes, associated to measurements by quasi-convex functions. Topological features of these complexes are then used to infer the intrinsic dimension. We prove convergence theorems that guarantee obtaining the correct intrinsic dimension in the limit of large data, under natural assumptions. We also illustrate the usability of this method in simulations.

 

Animals must learn to ignore stimuli that are irrelevant to survival and attend to ones that enhance survival. When a stimulus regularly fails to be associated with an important consequence, subsequent excitatory learning about that stimulus can be delayed, which is a form of nonassociative conditioning called ‘latent inhibition’. Honey bees show latent inhibition toward an odor they have experienced without association with food reinforcement. Moreover, individual honey bees from the same colony differ in the degree to which they show latent inhibition, and these individual differences have a genetic basis. To investigate the mechanisms that underly individual differences in latent inhibition, we selected two honey bee lines for high and low latent inhibition, respectively. We crossed those lines and mapped a Quantitative Trait Locus for latent inhibition to a region of the genome that contains the tyramine receptor geneAmtyr1[We use Amtyr1 to denote the gene and AmTYR1 the receptor throughout the text.]. We then show that disruption ofAmtyr1signaling either pharmacologically or through RNAi qualitatively changes the expression of latent inhibition but has little or slight effects on appetitive conditioning, and these results suggest that AmTYR1 modulates inhibitory processing in the CNS. Electrophysiological recordings from the brain during pharmacological blockade are consistent with a model that AmTYR1 indirectly regulates at inhibitory synapses in the CNS. Our results therefore identify a distinctAmtyr1-based modulatory pathway for this type of nonassociative learning, and we propose a model for howAmtyr1acts as a gain control to modulate hebbian plasticity at defined synapses in the CNS. We have shown elsewhere how this modulation also underlies potentially adaptive intracolonial learning differences among individuals that benefit colony survival. Finally, our neural model suggests a mechanism for the broad pleiotropy this gene has on several different behaviors.

 

To understand the operation of the olfactory system, it is essential to know how information is encoded in the olfactory bulb. We applied Shannon information theoretic methods to address this, with signals from up to 57 glomeruli simultaneously optically imaged from presynaptic inputs in glomeruli in the mouse dorsal (dOB) and lateral (lOB) olfactory bulb, in response to six exemplar pure chemical odors. We discovered that, first, the tuning of these signals from glomeruli to a set of odors is remarkably broad, with a mean sparseness of 0.83 and a mean signal correlation of 0.64. Second, both of these factors contribute to the low information that is available from the responses of even populations of many tens of glomeruli, which was only 1.35 bits across 33 glomeruli on average, compared with the 2.58 bits required to perfectly encode these six odors. Third, although there is considerable interest in the possibility of temporal encoding of stimulus including odor identity, the amount of information in the temporal aspects of the presynaptic glomerular responses was low (mean 0.11 bits) and, importantly, was redundant with respect to the information available from the rates. Fourth, the information from simultaneously recorded glomeruli asymptotes very gradually and nonlinearly, showing that glomeruli do not have independent responses. Fifth, the information from a population became available quite rapidly, within 100 ms of sniff onset, and the peak of the glomerular response was at 200 ms. Sixth, the information from the lOB was not additive with that of the dOB. NEW & NOTEWORTHY We report broad tuning and low odor information available across the lateral and dorsal bulb populations of glomeruli. Even though response latencies can be significantly predictive of stimulus identity, such contained very little information and none that was not redundant with information based on rate coding alone. Last, in line with the emerging notion of the important role of earliest stages of responses (“primacy”), we report a very rapid rise in information after each inhalation. 

In nature, olfactory signals are delivered to detectors—for example, insect antennae—by means of turbulent air, which exerts concurrent chemical and mechanical stimulation on the detectors. The antennal lobe, which is traditionally viewed as a chemosensory module, sits downstream of antennal inputs. We review experimental evidence showing that, in addition to being a chemosensory structure, antennal lobe neurons also respond to mechanosensory input in the form of wind speed. Benchmarked with empirical data, we constructed a dynamical model to simulate bimodal integration in the antennal lobe, with model dynamics yielding insights such as a positive correlation between the strength of mechanical input and the capacity to follow high frequency odor pulses, an important task in tracking odor sources. Furthermore, we combine experimental and theoretical results to develop a conceptual framework for viewing the functional significance of sensory integration within the antennal lobe. We formulate the testable hypothesis that the antennal lobe alternates between two distinct dynamical regimes, one which benefits odor plume tracking and one which promotes odor discrimination. We postulate that the strength of mechanical input, which correlates with behavioral contexts such being mid-flight versus hovering near a flower, triggers the transition from one regime to the other.