Interhemispheric connections between olfactory bulbs improve odor detection

Abstract

Interhemispheric connections enable interaction and integration of sensory information in bilaterian nervous systems and are thought to optimize sensory computations. However, the cellular and spatial organization of interhemispheric networks and the computational properties they mediate in vertebrates are still poorly understood. Thus, it remains unclear to what extent the connectivity between left and right brain hemispheres participates in sensory processing. Here, we show that the zebrafish olfactory bulbs (OBs) receive direct interhemispheric projections from their contralateral counterparts in addition to top-down inputs from the contralateral zebrafish homolog of olfactory cortex. The direct interhemispheric projections between the OBs reach peripheral layers of the contralateral OB and retain a precise topographic organization, which directly connects similarly tuned olfactory glomeruli across hemispheres. In contrast, interhemispheric top-down inputs consist of diffuse projections that broadly innervate the inhibitory granule cell layer. Jointly, these interhemispheric connections elicit a balance of topographically organized excitation and nontopographic inhibition on the contralateral OB and modulate odor responses. We show that the interhemispheric connections in the olfactory system enable the modulation of odor response and contribute to a small but significant improvement in the detection of a reproductive pheromone when presented together with complex olfactory cues by potentiating the response of the pheromone selective neurons. Taken together, our data show a previously unknown function for an interhemispheric connection between chemosensory maps of the olfactory system.

Stimulus-specific behavioral responses of zebrafish to a large range of odors exhibit individual variability

“…To explore how the stereotyped behavioral responses to odors relate to their internal representations in the olfactory system, we measured the response of the dorsal olfactory bulb to a subset of stimuli at the same behaviorally relevant concentrations. Patterns of neural activity evoked by different categories of odors are coarsely spatially organized in the ventral parts of the zebrafish olfactory bulb [6,11,14,65,66]. On the dorsal olfactory bulb, we found that bile acids strongly activated the medial parts, in accordance with previous studies in juvenile zebrafish [12].…”

“…The alarm odors, skin extract and conspecific blood, activate spatially overlapping olfactory bulb domains Our behavioral data suggest that zebrafish can smell blood and exhibit defensive behaviors that are similar to responses induced by the commonly used alarm odor, skin extract. To investigate whether conspecific blood activates the zebrafish olfactory system, we measured olfactory bulb responses to a subset of our odors, using two-photon calcium imaging in a brain explant preparation of Tg(elavl3:GCaMP6s) adult zebrafish [6,11,41,42] (see the "Methods" section). We found that both blood and skin extract specifically activated a subset of olfactory bulb neurons located in the anterolateral domain, below the dorsal surface of the olfactory bulb (Fig.…”

“…Chondroitin sulfate was diluted the morning of the experiment as previously described [31], to avoid damage of this heavy molecule by freezing the stock solutions. Olfactory stimuli for calcium imaging of OB responses consisted in blood, skin extract, taurocholic acid, and food extract diluted in artificial cerebrospinal fluid (ACSF [6]) at the same concentration as for the behavioral assays.…”

“…Odors are powerful drivers of a wide range of behavioral responses in fish, such as reproduction, foraging, and defensive behaviors [1][2][3]. The neural pathways underlying these stereotyped behaviors have been the focus of extensive research and are well described [4][5][6][7][8][9][10][11][12][13][14][15]. In the sea lampreys, a neural pathway comprising the olfactory bulb, posterior tuberculum, and mesencephalic locomotor region converts olfactory inputs into locomotor outputs by activating conserved brainstem pre-motor neurons (the reticulospinal neurons) [16][17][18][19], which in turn control the spinal cord locomotor centers [4].…”

LRR-Containing Oncofetal Trophoblast Glycoprotein 5T4 Shapes Neural Circuits in Olfactory and Visual Systems

“…Recently, it was reported that zebrafish MCs receive direct interhemispheric projections from their contralateral counterparts, whereas interneurons receive interhemispheric top-down inputs from the contralateral zebrafish homolog of the olfactory cortex (Kermen et al, 2020). Mouse MCs/TCs receive indirect interhemispheric projections from their contralateral counterparts via the anterior olfactory nucleus pars externa (Grobman et al, 2018), whereas interneurons receive top-down inputs mostly from the ipsilateral olfactory cortex (Niedworok et al, 2012).…”