Non-preferred contrast responses in the Drosophila motion pathways reveal a receptive field structure that explains a common visual illusion

Gruntman, Eyal; Reimers, Pablo; Romani, Sandro; Reiser, Michael B.

doi:10.1016/j.cub.2021.09.072

Cited by 8 publications

(7 citation statements)

References 61 publications

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“…The response time traces revealed that T4 responds to light bars (its preferred contrast, PC), but also to dark ones (its non-preferred contrast, NC), while T5 responds to dark bars (its PC), but also to light ones (its NC) ( Fig. 7A ), in agreement a prior report 76 . For both T4 and T5, the peak time in responses to NC stimuli is delayed compared to the peak time to PC stimuli, reminiscent to the responses measured in neurons upstream of T4 and T5 ( Fig.…”

Section: Resultssupporting

confidence: 91%

“…7 ). This is in agreement with a prior report that T4 and T5 respond to bars of their non-preferred contrast 76 . Importantly, our data show that these properties depend critically on the sparsity of the stimulus ( Fig.…”

Section: Discussionsupporting

confidence: 94%

“…7D, F ) — for instance, in dense stimuli, T4 and T5 neurons are not activated by their non-preferred contrast. Moreover, the responses in T4 and T5 mirror the response properties of cells upstream of T4 and T5, suggesting that they inherit many of these properties and do not require distinct conductances to generate them, as was proposed to explain the earlier observation 76 ( Fig. 6 ).…”

Section: Discussionmentioning

confidence: 53%

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Adaptation to visual sparsity enhances responses to infrequent stimuli

Gou,

Matulis,

Clark

2024

Preprint

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Sensory systems adapt their response properties to the statistics of their inputs. For instance, visual systems adapt to low-order statistics like mean and variance to encode the stimulus efficiently or to facilitate specific downstream computations. However, it remains unclear how other statistical features affect sensory adaptation. Here, we explore how Drosophila's visual motion circuits adapt to stimulus sparsity, a measure of the signal's intermittency not captured by low-order statistics alone. Early visual neurons in both ON and OFF pathways alter their responses dramatically with stimulus sparsity, responding positively to both light and dark sparse stimuli but linearly to dense stimuli. These changes extend to downstream ON and OFF direction-selective neurons, which are activated by sparse stimuli of both polarities, but respond with opposite signs to light and dark regions of dense stimuli. Thus, sparse stimuli activate both ON and OFF pathways, recruiting a larger fraction of the circuit and potentially enhancing the salience of infrequent stimuli. Overall, our results reveal visual response properties that increase the fraction of the circuit responding to sparse, infrequent stimuli.

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Section: Resultssupporting

confidence: 91%

Section: Discussionsupporting

confidence: 94%

Section: Discussionmentioning

confidence: 53%

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Adaptation to visual sparsity enhances responses to infrequent stimuli

Gou,

Matulis,

Clark

2024

Preprint

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“…Other neurons in the adult Drosophila brain have also been identified as nonspiking. For instance, a variety of neurons, including interneurons, in the fly visual system are nonspiking ( Behnia et al, 2014 ; Gruntman et al, 2021 ; Kohn et al, 2021 ). The lack of action potentials in these neurons may facilitate local processing and allow fewer neurons in the invertebrate CNS to perform the role of multiple cell classes in animals with a greater number of neurons.…”

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Nonspiking Interneurons in theDrosophilaAntennal Lobe Exhibit Spatially Restricted Activity

Schenk

Gaudry

2023

eNeuro

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Inhibitory interneurons are important for neuronal circuit function. They regulate sensory inputs and enhance output discriminability (Olsen et al., 2010; Olsen and Wilson, 2008; Root et al., 2008). Often, the identities of interneurons can be determined by location and morphology, which can have implications for their functions (Wachowiak and Shipley, 2006). While most interneurons fire traditional action potentials, many are nonspiking. These can be seen in insect olfaction (Husch et al., 2009; Laurent and Davidowitz, 1994; Tabuchi et al., 2015) and the vertebrate retina (Gleason et al., 1993). Here, we present the novel observation of nonspiking inhibitory interneurons in the antennal lobe (AL) of the adult fruit fly,Drosophila melanogaster. These neurons have a morphology where they innervate a patchwork of glomeruli. We used electrophysiology to determine if their nonspiking characteristic is due to a lack of sodium current. We then used immunohistochemsitry andin situhybridization to show this is likely achieved through translational regulation of the voltage gated sodium channel gene,para. Usingin vivocalcium imaging, we explored how these cells respond to odors, finding regional isolation in their responses' spatial patterns. Further, their response patterns were dependent on both odor identity and concentration. Thus, we surmise these neurons are electrotonically compartmentalized such that activation of the neurites in one region does not propagate across the whole antennal lobe. We propose these neurons may be the source of intraglomerular inhibition in the AL and may contribute to regulation of spontaneous activity within glomeruli.Significance StatementThese findings are a novel discovery of nonspiking interneurons specifically in the olfactory system of adultDrosophila melanogaster. The role of the nonspiking characteristic of similar interneurons in other species is not fully understood. Further, the sources of specific regulatory mechanisms such as intraglomerular inhibition in the fly are unclear. The characterization of nonspiking interneurons inDrosophilabegins to explain these mechanisms and provides an avenue for further study into the roles of similar cells across species.

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