How auditory selectivity for sound timing arises: The diverse roles of GABAergic inhibition in shaping the excitation to interval-selective midbrain neurons

Alluri, Rishi K.; Rose, Garrett S.; Leary, Christopher J.; Palaparthi, Anil; Hanson, Jessica L.; Vasquez-Opazo, Gustavo A.; Graham, Jalina A.; Luong, Kyphuong

doi:10.1016/j.pneurobio.2020.101962

Cited by 11 publications

(10 citation statements)

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“…From published studies [ 61 , 64 , 65 , 67 , 68 ], we identified 39 target protein families associated with synaptic transmission (Table 1 ; Methods—Identification of Candidate Gene Transcripts Involved in Synaptic Transmission ). We obtained matches to 97% (38 of 39) of these target protein families in the expression transcriptome: 1104 (~ 2%) of reference transcripts contained one or more keywords.…”

Section: Resultsmentioning

confidence: 99%

“…These differences may be mediated by divergence in genes and/or their expression that govern the presence and function of inhibitory and excitatory synapses. For example, up-regulation of one or more genes that encode GABAergic receptors in ICNs may increase the relative amplitude of inhibition and as a consequence increase the number of pulses required for eliciting responses [ 64 , 65 ] (G. Rose, unpublished observations). Thus, changes in expression of ionotropic receptor genes and other genes related to synaptic transmission might underlie the observed differences in mating behaviors between ancestral and reinforced populations.…”

Section: Introductionmentioning

confidence: 99%

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Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)

et al. 2021

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Background Species interactions can promote mating behavior divergence, particularly when these interactions are costly due to maladaptive hybridization. Selection against hybridization can indirectly cause evolution of reproductive isolation within species, a process termed cascade reinforcement. This process can drive incipient speciation by generating divergent selection pressures among populations that interact with different species assemblages. Theoretical and empirical studies indicate that divergent selection on gene expression networks has the potential to increase reproductive isolation among populations. After identifying candidate synaptic transmission genes derived from neurophysiological studies in anurans, we test for divergence of gene expression in a system undergoing cascade reinforcement, the Upland Chorus Frog (Pseudacris feriarum). Results Our analyses identified seven candidate synaptic transmission genes that have diverged between ancestral and reinforced populations of P. feriarum, including five that encode synaptic vesicle proteins. Our gene correlation network analyses revealed four genetic modules that have diverged between these populations, two possessing a significant concentration of neurotransmission enrichment terms: one for synaptic membrane components and the other for metabolism of the neurotransmitter nitric oxide. We also ascertained that a greater number of genes have diverged in expression by geography than by sex. Moreover, we found that more genes have diverged within females as compared to males between populations. Conversely, we observed no difference in the number of differentially-expressed genes within the ancestral compared to the reinforced population between the sexes. Conclusions This work is consistent with the idea that divergent selection on mating behaviors via cascade reinforcement contributed to evolution of gene expression in P. feriarum. Although our study design does not allow us to fully rule out the influence of environment and demography, the fact that more genes diverged in females than males points to a role for cascade reinforcement. Our discoveries of divergent candidate genes and gene networks related to neurotransmission support the idea that neural mechanisms of acoustic mating behaviors have diverged between populations, and agree with previous neurophysiological studies in frogs. Increasing support for this hypothesis, however, will require additional experiments under common garden conditions. Our work points to the importance of future replicated and tissue-specific studies to elucidate the relative contribution of gene expression divergence to the evolution of reproductive isolation during incipient speciation.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)

et al. 2021

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“…Finally, a negative current (~ 0.5 nA) was applied to rupture a tiny portion of the cell. Additional details on whole-cell recording procedures can be found elsewhere (Alluri et al, 2016(Alluri et al, , 2021 After isolating a single unit, we determined the unit's best excitatory frequency (BEF) as the carrier frequency that elicited a response at the lowest threshold, where threshold was defined as the sound pressure level at which a unit spiked in response to at least 50% of the stimulus presentations. All subsequent acoustic stimuli used to record from that unit were generated at the unit's BEF and were broadcast at amplitudes ~10 dB above the unit's threshold.…”

Section: Stimulus Generation and Presentationmentioning

confidence: 99%

Neural Basis of Acoustic Species Recognition in a Cryptic Species Complex

Gupta

Alluri

Rose

et al. 2021

Preprint

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Sexual traits that promote species recognition are important drivers of reproductive isolation, especially among closely related species. Identifying neural processes that shape species differences in recognition is crucial for understanding the causal mechanisms of reproductive isolation. Temporal patterns are salient features of sexual signals that are widely used in species recognition by several taxa, including anurans. Recent advances in our understanding of temporal processing by the anuran auditory system provide an excellent opportunity to investigate the neural basis of species-specific recognition. The anuran inferior colliculus (IC) consists of neurons that are selective for temporal features of calls. Of potential relevance are auditory neurons known as interval-counting neurons (ICNs) that are often selective for the pulse rate of conspecific advertisement calls. Here, we took advantage of a species differences in temporal selectivity for pulsatile advertisement calls exhibited by two cryptic species of gray treefrog (Hyla chrysoscelis and Hyla versicolor) to test the hypothesis that ICNs mediate acoustic species recognition. We tested this hypothesis by examining the extent to which the threshold number of pulses required to elicit behavioral responses from females and neural responses from ICNs was similar within each species but potentially different between the two species. In support of our hypothesis, we found that a species difference in behavioral pulse number thresholds corresponded closely to a parallel species difference in neural pulse number thresholds. However, this relationship held only for ICNs that exhibited band-pass tuning for conspecific pulse rates. Together, these findings suggest that differences in temporal processing of a subset of ICNs provide a mechanistic explanation for reproductive isolation between two cryptic and syntopically breeding treefrog species.

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“…The parameters underlying sparse coding of cortical circuits are not fully understood. Unbalanced synaptic excitatory and inhibitory is known to underlie sparse coding in cortical populations [29]. Another parameter is the connectivity in the cortex as an important feature of efficient sensory encoding [29], [30].…”

Section: Introductionmentioning

confidence: 99%

“…Unbalanced synaptic excitatory and inhibitory is known to underlie sparse coding in cortical populations [29]. Another parameter is the connectivity in the cortex as an important feature of efficient sensory encoding [29], [30]. Deep sparse coding neural networks have been developed by combining convolutional neural networks (CNNs) and sparse coding techniques for image feature extraction [31], [32] or speech recognition [33].…”

Section: Introductionmentioning

confidence: 99%

A Neuroscience-Inspired Spiking Neural Network for Auditory Spatial Attention Detection Using Single-Trial EEG

Faghihi

Cai

Moustafa

2021

Preprint

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Recently, studies have shown that the alpha band (8-13 Hz) EEG signals enable the decoding of auditory spatial attention. However, deep learning methods typically requires a large amount of training data. Inspired by sparse coding in cortical neurons, we propose a spiking neural network model for auditory spatial attention detection. The model is composed of three neural layers, two of them are spiking neurons. We formulate a new learning rule that is based on firing rate of pre synaptic and post-synaptic neurons in the first layer and the second layer of spiking neurons. The third layer consists of 10 spiking neurons that the pattern of their firing rate after training is used in test phase of the method. The proposed method extracts the patterns of recorded EEG of leftward and rightward attention, independently, and uses them to train network to detect the auditory spatial attention. In addition, a computational approach is presented to find the best single-trial EEG data as training samples of leftward and rightward attention EEG. In this model, the role of using low connectivity rate of the layers and specific range of learning parameters in sparse coding is studied. Importantly, unlike most prior model, our method requires 10% of EEG data as training data and has shown 90% accuracy in average. This study suggests new insights into the role of sparse coding in both biological networks and brain-inspired machine learning.

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How auditory selectivity for sound timing arises: The diverse roles of GABAergic inhibition in shaping the excitation to interval-selective midbrain neurons

Cited by 11 publications

References 42 publications

Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)

Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)

Neural Basis of Acoustic Species Recognition in a Cryptic Species Complex

A Neuroscience-Inspired Spiking Neural Network for Auditory Spatial Attention Detection Using Single-Trial EEG

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