Multiple network properties overcome random connectivity to enable stereotypic sensory responses

Mittal, Aarush Mohit; Gupta, Diksha; Singh, Amrita; Lin, Andrew C.; Gupta, Nitin

doi:10.1038/s41467-020-14836-6

Cited by 15 publications

(15 citation statements)

References 79 publications

(164 reference statements)

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“…Random connectivity between OB and OC neurons 10-12 makes the task of achieving perceptual unity more difficult. One way of overcoming this randomness in connections has been suggested in recent modeling studies 88,89 . The idea is that two neurons, each located downstream of PC neurons in a different hemisphere, can have similar odor receptive fields, despite the variability in the OB-OC connections in the two hemispheres, if they integrate odor information from a large number of OC neurons.…”

Section: How Is Perceptual Unity Achieved In Olfaction?mentioning

confidence: 99%

Bilateral and unilateral odor processing and odor perception

2020

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Imagine smelling a novel perfume with only one nostril and then smelling it again with the other nostril. Clearly, you can tell that it is the same perfume both times. This simple experiment demonstrates that odor information is shared across both hemispheres to enable perceptual unity. In many sensory systems, perceptual unity is believed to be mediated by inter-hemispheric connections between iso-functional cortical regions. However, in the olfactory system, the underlying neural mechanisms that enable this coordination are unclear because the two olfactory cortices are not topographically organized and do not seem to have homotypic inter-hemispheric mapping. This review presents recent advances in determining which aspects of odor information are processed unilaterally or bilaterally, and how odor information is shared across the two hemispheres. We argue that understanding the mechanisms of inter-hemispheric coordination can provide valuable insights that are hard to achieve when focusing on one hemisphere alone. I n the early 1940s, patients suffering from severe untreatable epileptic seizures underwent a pioneering operation in which their corpus callosum was severed. While this mitigated the epilepsy syndromes, it generated strange phenomena: each hemisphere seemed to have its own separate perception, concepts, and even actions. When such split-brain patients were shown an image of an object in their left visual field, they could not vocally name what they had seen. This is because information about the image seen in the left visual field is sent only to the right side of the brain, while the speech-control center is usually on the left side of the brain. Nonetheless, patients could pick up the correct object with their left hand because it is controlled by the right hemisphere 1. Some of the surgery-induced deficits improved over time, but they illustrate one important principle: the fibers that interconnect the hemispheres are responsible for transferring information from one side to the other. These connecting fibers may be required to achieve perceptual unity, at least in some sensory modalities. But how is perceptual unity achieved? There are several possible ways to achieve perceptual unity in the healthy brain. One way is to ensure that sensory information is transmitted to both hemispheres directly from the sensory organs. This is how auditory information is unified across hemispheres: information from both ears converges to the left and the right Superior Olivary

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Section: How Is Perceptual Unity Achieved In Olfaction?mentioning

confidence: 99%

Bilateral and unilateral odor processing and odor perception

2020

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“…The authors investigated a CN2 cell type and found it to be excited by appetitive LHNs and MBONs and inhibited by aversive MBONs. Naive MBON activity is likely to be relatively stereotyped between animals (Mittal et al, 2020). The hypothesis is that in naive animals, opposing MBON drive balances to produce a stereotyped 'innate' outcome; learning then shifts this balance to bias behaviour.…”

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confidence: 99%

Information flow, cell types and stereotypy in a full olfactory connectome

Schlegel

Bates

Stürner

et al. 2020

Preprint

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The hemibrain connectome (Scheffer et al., 2020) provides large scale connectivity and morphology information for the majority of the central brain of Drosophila melanogaster. Using this data set, we provide a complete description of the most complex olfactory system studied at synaptic resolution to date, covering all first, second and third-order neurons of the olfactory system associated with the antennal lobe and lateral horn (mushroom body neurons are described in a parallel paper, (Li et al., 2020)). We develop a generally applicable strategy to extract information flow and layered organisation from synaptic resolution connectome graphs, mapping olfactory input to descending interneurons. This identifies a range of motifs including highly lateralised circuits in the antennal lobe and patterns of convergence downstream of the mushroom body and lateral horn. We also leverage a second data set (FAFB, (Zheng et al., 2018)) to provide a first quantitative assessment of inter- versus intra-individual stereotypy. Complete reconstruction of select developmental lineages in two brains (three brain hemispheres) reveals striking similarity in neuronal morphology across brains for >170 cell types. Within and across brains, connectivity correlates with morphology. Notably, neurons of the same morphological type show similar connection variability within one brain as across brains; this property should enable a rigorous quantitative approach to cell typing.

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“…We checked whether the population of mALT PNs from each MGC unit showed consistent responses across individual insects. The response consistency of a group of PNs can be quantified as the Pearson’s correlation coefficient of the response vectors in two individual insects, where each vector contains the trial-averaged responses of an individual to a given set of odors ( Mittal et al, 2020 ; Schaffer et al, 2018 ). The average correlation between the cumulus medial-tract PNs responses (mean calcium signal during stimulation windows subtracted by that during the pre-stimulation period) across individuals was 0.45.…”

Section: Resultsmentioning

confidence: 99%

Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain

Kymre

Liu

Ian

et al. 2021

eLife

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The pheromone system of heliothine moths is an optimal model for studying principles underlying higher-order olfactory processing. In Helicoverpa armigera, three male-specific glomeruli receive input about three female-produced signals, the primary pheromone component, serving as an attractant, and two minor constituents, serving a dual function, i.e. attraction versus inhibition of attraction. From the antennal-lobe glomeruli, the information is conveyed to higher olfactory centers, including the lateral protocerebrum, via three main paths – of which the medial tract is the most prominent. In this study, we traced physiologically identified medial-tract projection neurons from each of the three male‑specific glomeruli with the aim of mapping their terminal branches in the lateral protocerebrum. Our data suggest that the neurons’ wide-spread projections are organized according to behavioral significance, including a spatial separation of signals representing attraction versus inhibition – however, with a unique capacity of switching behavioral consequence based on the amount of the minor components.

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Multiple network properties overcome random connectivity to enable stereotypic sensory responses

Cited by 15 publications

References 79 publications

Bilateral and unilateral odor processing and odor perception

Bilateral and unilateral odor processing and odor perception

Information flow, cell types and stereotypy in a full olfactory connectome

Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain

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