Life Sciences Commons^™

Community-Derived Core Concepts For Neuroscience Higher Education, Audrey Chen, Kimberley A. Phillips, Jennifer E. Schaefer, Patrick M. Sonner

Biology Faculty Publications

Core concepts provide a framework for organizing facts and understanding in neuroscience higher education curricula. Core concepts are overarching principles that identify patterns in neuroscience processes and phenomena and can be used as a foundational scaffold for neuroscience knowledge. The need for community-derived core concepts is pressing, because both the pace of research and number of neuroscience programs are rapidly expanding. While general biology and many subdisciplines within biology have identified core concepts, neuroscience has yet to establish a community-derived set of core concepts for neuroscience higher education. We used an empirical approach involving more than 100 neuroscience educators to …

Glia Excitation In The Cns Modulates Intact Behaviors And Sensory-Cns-Motor Circuitry, Shelby Mccubbin, Douglas A. Harrison, Robin L. Cooper

Biology Faculty Publications

Glial cells play a role in many important processes, though the mechanisms through which they affect neighboring cells are not fully known. Insights may be gained by selectively activating glial cell populations in intact organisms utilizing the activatable channel proteins channel rhodopsin (ChR2XXL) and TRPA1. Here, the impacts of the glial-specific expression of these channels were examined in both larval and adult Drosophila. The Glia > ChR2XXL adults and larvae became immobile when exposed to blue light and TRPA1-expressed Drosophila upon heat exposure. The chloride pump expression in glia > eNpHR animals showed no observable differences in adults or larvae. In …

The Effect Of Optogenetically Activating Glia On Neuronal Function, Cecilia Pankau, Shelby Mccubbin, Robin L. Cooper

Biology Faculty Publications

Glia, or glial cells, are considered a vital component of the nervous system, serving as an electrical insulator and a protective barrier from the interstitial (extracellular) media. Certain glial cells (i.e., astrocytes, microglia, and oligodendrocytes) within the CNS have been shown to directly affect neural functions, but these properties are challenging to study due to the difficulty involved with selectively-activating specific glia. To overcome this hurdle, we selectively expressed light-sensitive ion channels (i.e., channel rhodopsin, ChR2-XXL) in glia of larvae and adult Drosophila melanogaster. Upon activation of ChR2, both adults and larvae showed a rapid contracture of body wall …

The Effect Of Calcium Ions On Mechanosensation And Neuronal Activity In Proprioceptive Neurons, Devan E. Atkins, Kimberly L. Bosh, Grace W. Breakfield, Sydney E. Daniels, Makayla J. Devore, Hailey E. Fite, Landys Z. Guo, Danielle K. J. Henry, Alana K. Kaffenberger, Katherine S. Manning, Tatum E. Mowery, Cecilia L. Pankau, Nyla Parker, Malina E. Serrano, Yamaan Shakhashiro, Hannah N. Tanner, Ruth. A. Ward, Aubrey H. Wehry, Robin L. Cooper

Biology Faculty Publications

Proprioception of all animals is important in being able to have coordinated locomotion. Stretch activated ion channels (SACs) transduce the mechanical force into electrical signals in the proprioceptive sensory endings. The types of SACs vary among sensory neurons in animals as defined by pharmacological, physiological and molecular identification. The chordotonal organs within insects and crustaceans offer a unique ability to investigate proprioceptive function. The effects of the extracellular environment on neuronal activity, as well as the function of associated SACs are easily accessible and viable in minimal saline for ease in experimentation. The effect of extracellular [Ca²⁺] on …

Gephyrin-Lacking Pv Synapses On Neocortical Pyramidal Neurons, Dika A. Kuljis, Kristina D. Micheva, Ajit Ray, Waja Wegner, Ryan Bowman, Daniel V. Madison, Katrin I. Willig, Alison L. Barth

Biology Faculty Publications

Gephyrin has long been thought of as a master regulator for inhibitory synapses, acting as a scaffold to organize γ-aminobutyric acid type A receptors (GABA_ARs) at the post-synaptic density. Accordingly, gephyrin immunostaining has been used as an indicator of inhibitory synapses; despite this, the pan-synaptic localization of gephyrin to specific classes of inhibitory synapses has not been demonstrated. Genetically encoded fibronectin intrabodies generated with mRNA display (FingRs) against gephyrin (Gephyrin.FingR) reliably label endogenous gephyrin, and can be tagged with fluorophores for comprehensive synaptic quantitation and monitoring. Here we investigated input- and target-specific localization of gephyrin at a defined …

A Two-Clone Approach To Study Signaling Interactions Among Neuronal Cells In A Pre-Clinical Alzheimer’S Disease Model, Catherine J. Yeates, Ankita Sarkar, Prajakta Deshpande, Madhuri Kango-Singh, Amit Singh

Biology Faculty Publications

To understand the progression of Alzheimer's disease, studies often rely on ectopic expression of amyloid-beta 42 (Aβ42) throughout an entire tissue. Uniform ectopic expression of Aβ42 may obscure cell-cell interactions that contribute to the progression of the disease. We developed a two-clone system to study the signaling cross talk between GFP-labeled clones of Aβ42-expressing neurons and wild-type neurons simultaneously generated from the same progenitor cell by a single recombination event. Surprisingly, wild-type clones are reduced in size as compared with Aβ42-producing clones. We found that wild-type cells are eliminated by the induction of cell death. Furthermore, aberrant activation of c-Jun-N-terminal …

Her9/Hes4 Is Required For Retinal Photoreceptor Development, Maintenance, And Survival, Cagney E. Coomer, Stephen G. Wilson, Kayla F. Titialii-Torres, Jessica D. Bills, Laura A. Krueger, Rebecca A. Petersen, Evelyn M. Turnbaugh, Eden L. Janesch, Ann C. Morris

Biology Faculty Publications

The intrinsic and extrinsic factors that regulate vertebrate photoreceptor specification and differentiation are complex, and our understanding of all the players is far from complete. Her9, the zebrafish ortholog of human HES4, is a basic helix-loop-helix-orange transcriptional repressor that regulates neurogenesis in several developmental contexts. We have previously shown that her9 is upregulated during chronic rod photoreceptor degeneration and regeneration in adult zebrafish, but little is known about the role of her9 during retinal development. To better understand the function of Her9 in the retina, we generated zebrafish her9 CRISPR mutants. Her9 homozygous mutants displayed striking retinal phenotypes, including decreased …

The Effects Of Bacterial Endotoxin Lps On Synaptic Transmission At The Neuromuscular Junction, Robin L. Cooper, Micaiah Mcnabb, Jeremy Nadolski

Biology Faculty Publications

The direct action of bacterial lipopolysaccharides (LPS) endotoxin was shown to enhance synaptic transmission and hyperpolarize the membrane potential at low doses, but block glutamatergic receptors and decrease observable spontaneous events at a high dosage. The dosage effects are LPS type specific. The hyperpolarization is not due to voltage-gated potassium channels or to activation of nitric oxide synthase (NOS). The effects are induced directly by LPS, independent of an immune response.

A Cross-Species Analysis Reveals A General Role For Piezo2 In Mechanosensory Specialization Of Trigeminal Ganglia From Tactile Specialist Birds, Eve R. Schneider, Evan O. Anderson, Viktor V. Feketa, Marco Mastrotto, Yury A. Nikolaev, Elena O. Gracheva, Sviatoslav N. Bagriantsev

Biology Faculty Publications

A major challenge in biology is to link cellular and molecular variations with behavioral phenotypes. Here, we studied somatosensory neurons from a panel of bird species from the family Anatidae, known for their tactile-based foraging behavior. We found that tactile specialists exhibit a proportional expansion of neuronal mechanoreceptors in trigeminal ganglia. The expansion of mechanoreceptors occurs via neurons with intermediately and slowly inactivating mechanocurrent. Such neurons contain the mechanically gated Piezo2 ion channel whose expression positively correlates with the expression of factors responsible for the development and function of mechanoreceptors. Conversely, Piezo2 expression negatively correlates with expression of molecules mediating …

Nell2 Regulates The Contralateral-Versus-Ipsilateral Visual Projection As A Domain-Specific Positional Cue, Chizu Nakamoto, Elaine Durward, Masato Horie, Masaru Nakamoto

Biology Faculty Publications

In mammals with binocular vision, retinal ganglion cell (RGC) axons from each eye project to eye-specific domains in the contralateral and ipsilateral dorsal lateral geniculate nucleus (dLGN), underpinning disparity-based stereopsis. Although domain-specific axon guidance cues that discriminate contralateral and ipsilateral RGC axons have long been postulated as a key mechanism for development of the eye-specific retinogeniculate projection, the molecular nature of such cues has remained elusive. Here, we show that the extracellular glycoprotein Nell2 (neural epidermal growth factor-like-like 2) is expressed in the dorsomedial region of the dLGN, which ipsilateral RGC axons terminate in and contralateral axons avoid. In Nell2 …

The Premammillary Nucleus Of The Hypothalamus Is Not Necessary For Photoperiodic Timekeeping In Female Turkeys (Meleagris Gallopavo), Ashli F. Moore, Vincent M. Cassone, Kevin D. Alloway, Paul A. Bartell

Biology Faculty Publications

In birds, seasonal reproduction is regulated by day length, with long days in the spring activating the hypothalamic-pituitary-gonadal axis and reproductive behaviors. The photoreceptors mediating this process remain unknown, but recently, the premammillary nucleus (PMM) of the hypothalamus has been implicated as the site of photoperiodic signaling in turkeys. We performed electrolytic lesions of the PMM to elucidate its role in the photoactivation and maintenance of egg production in female turkeys. Our results show that ablation of the PMM does not alter the normal lay cycle. No differences were found between lesioned birds and sham controls in the latency to …

Effects Of Clove Oil (Eugenol) On Proprioceptive Neurons, Heart Rate, And Behavior In Model Crustaceans, Samuel Wycoff, Kristin Weineck, Shannon Conlin, Chinni Suryadevara, Elizabeth Grau, Alec Bradley, Danielle Cantrell, Samantha Eversole, Carolyn Grachen, Kaylee Hall, Danielle Hawthorne, Claire Kinmon, Paula Ortiz Guerrero, Bhavik Patel, Kaitlyn Samuels, Gia Valdes, Andrew J. Ray, Leo J. Fleckenstein, Elena Piana, Robin L. Cooper

Biology Faculty Publications

Clove oil contains eugenol as an active ingredient and is used as a topical anesthetic in mammals to remedy pain and to anesthetize fish and other seafood for short periods; however, the exact mechanism of action of eugenol is not fully understood. We examined use of eugenol as a reversible anesthetic in crustaceans by examining its effect on sensory and motor neurons in the Red Swamp crayfish (Procambarus clarkii), Blue crab (Callinectes sapidus) and Whiteleg shrimp (Litopenaeus vannamei) with electrophysiological recordings. The neurogenic heart rate in the three species was also monitored along with …

Investigating The Effects Of Homocysteine As An Agonist On Invertebrate Glutamatergic Synapses, Elizabeth Grau, Alexandra E. Stanback, Alec Bradley, Danielle Cantrell, Samantha Eversole, Carolyn Grachen, Kaylee Hall, Danielle Hawthorne, Claire Kinmon, Paula Ortiz Guerrero, Bhavik Patel, Kaitlyn Samuels, Chinni Suryadevara, Gia Valdes, Samuel Wycoff, Robin L. Cooper

Biology Faculty Publications

Hyperhomocysteinemia (HHcy) in mammals can produce neurological deficits, such as memory loss. The cause of the neurological issues is assumed to be due to homocysteine (HCY) binding to glutamatergic receptors in the central nervous system (CNS). High levels of HCY in the CNS are also associated with Amyotrophic Lateral Sclerosis (ALS) and Parkinson’s disease. Thus, understanding the detailed mechanisms of HCY in model preparations could be useful in developing potential treatments to neurodegenerative diseases with overlapping symptoms to HHcy. The aim of this study is to investigate the efficacy of HCY as an agonist at glutamatergic synapses in invertebrates. The …

The Effect Of Co2, Intracellular Ph And Extracellular Ph On Mechanosensory Proprioceptor Responses In Crayfish And Crab, Viresh Dayaram, Cole A. Malloy, Sarah Martha, Brenda Alvarez, Ikenna Chukwudolue, Nadera Dabbain, Dlovan D.Mahmood, Slavina Goleva, Tori Hickey, Angel Ho, Molly King, Paige Kington, Matthew Mattingly, Samuel Potter, Landon Simpson, Amanda Spence, Henry Uradu, Jacob Van Doorn, Dlovan Faiq, Robin L. Cooper

Biology Faculty Publications

Proprioceptive neurons monitor the movements of limbs and joints to transduce the movements into electrical signals. These neurons function similarly in species from arthropods to humans. These neurons can be compromised in disease states and in adverse environmental conditions such as with changes in external and internal pH. We used two model preparations (the crayfish muscle receptor organ and a chordotonal organ in the limb of a crab) to characterize the responses of these proprioceptors to external and internal pH changes as well as raised CO₂. The results demonstrate the proprioceptive organs are not highly sensitive to changes …

A Novel Educational Module To Teach Neural Circuits For College And High School Students: Ngss-Neurons, Genetics, And Selective Stimulations, Zana R. Majeed, Felicitas Koch, Joshua Morgan, Heidi Anderson, Jennifer Wilson, Robin L. Cooper

Biology Faculty Publications

This report introduces various approaches to target defined neural pathways for stimulation and to address the effect of particular neural circuits on behavior in a model animal, the fruit fly (Drosophila melanogaster). The objective of this novel educational module described can be used to explain and address principle concepts in neurobiology for high school and college level students. A goal of neurobiology is to show how neural circuit activity controls corresponding behavior in animals. The fruit fly model system provides powerful genetic tools, such as the UAS-Gal4 system, to manipulate expression of non-native proteins in various populations of …

Stretch Activated Channels In Proprioceptive Organs Of Crab And Crayfish Are Sensitive To Gadolinium But Not Amiloride, Ruthenium Red Or Low Ph, Viresh Dayaram, Cole A. Malloy, Sarah Martha, Brenda Alvarez, Ikenna Chukwudolue, Nadera Dabbain, Dlovan D.Mahmood, Slavina Goleva, Tori Hickey, Angel Ho, Molly King, Paige Kington, Matthew Mattingly, Samuel Potter, Landon Simpson, Amanda Spence, Henry Uradu, Jacob Van Doorn, Robin L. Cooper

Biology Faculty Publications

The type of stretch activated receptors (SARs) in the chordotonal organs in the crab walking leg and of the muscle receptor organ (MRO) in the crayfish abdomen have not yet been classified as to their molecular or pharmacological profile. The purpose of this study is to examine the pharmacological profile of SARs in the proprioceptive neurons in the crab and crayfish models. Since many SARs share the pharmacological profile of displaying low pH or being proton sensitive (i.e. being more active) or blocked by the diuretic amiloride or ruthenium red as well as being blocked by the broad stretch activated …

Transposon-Mediated Stable Suppression Of Gene Expression In The Developing Chick Retina, Masaru Nakamoto, Chizu Nakamoto

Biology Faculty Publications

The embryonic chick has long been a favorite model system for in vivo studies of vertebrate development. However, a major technical limitation of the chick embryo has been the lack of efficient loss-of-function approaches for analyses of gene functions. Here, we describe a methodology in which a transgene encoding artificial microRNA sequences is introduced into embryonic chick retinal cells by in ovo electroporation and integrated into the genome using the Tol2 transposon system. We show that this methodology can induce potent and stable suppression of gene expression. This technique therefore provides a rapid and robust loss-of-function approach for studies of …

Glyphosate Induces Neurotoxicity In Zebrafish, Nicole M. Roy, Bruno Carneiro, Jeremy Ochs

Biology Faculty Publications

Glyphosate based herbicides (GBH) like Roundup^® are used extensively in agriculture as well as in urban and rural settings as a broad spectrum herbicide. Its mechanism of action was thought to be specific only to plants and thus considered safe and non-toxic. However, mounting evidence suggests that GBHs may not be as safe as once thought as initial studies in frogs suggest that GBHs may be teratogenic. Here we utilize the zebrafish vertebrate model system to study early effects of glyphosate exposure using technical grade glyphosate and the Roundup^® Classic formulation. We find morphological abnormalities including cephalic and …

Behavioral And Neural Indices Of Metacognitive Sensitivity In Preverbal Infants, Louise Goupil, Sid Kouider

Biology Faculty Publications

Humans adapt their behavior not only by observing the consequences of their actions but also by internally monitoring their performance. This capacity, termed metacognitive sensitivity [1 ; 2], has traditionally been denied to young children because they have poor capacities in verbally reporting their own mental states [3; 4 ; 5]. Yet, these observations might reflect children’s limited capacities for explicit self-reports, rather than limitations in metacognition per se. Indeed, metacognitive sensitivity has been shown to reflect simple computational mechanisms [1; 6; 7 ; 8], and can be found in various …

Evaluation Of The Developmental Toxicity Of Lead In The Danio Rerio Body, Nicole M. Roy, Sarah Dewolf, Bruno Carneiro

Biology Faculty Publications

Lead has been utilized throughout history and is widely distributed and mobilized globally. Although lead in the environment has been somewhat mitigated, the nature of lead and its extensive uses in the past prohibit it from being completely absent from our environment and exposure to lead is still a public health concern. Most studies regarding lead toxicity have focused on the brain. However, little is found in the literature on the effects of lead in other tissues. Here, we utilize the zebrafish model system to investigate effects of lead exposure during early developmental time windows at 24, 48 and 72 …

Lights And Larvae: Using Optogenetics To Teach Recombinant Dna And Neurobiology, John Titlow, Heidi Anderson, Robin L. Cooper

Biology Faculty Publications

Switching genes between organisms and controlling an animal’s brain using lasers may seem like science fiction, but with advancements in a technique called optogenetics, such experiments are now common in neuroscience research. Optogenetics combines recombinant DNA technology with a controlled light source to help researchers address biomedical questions in the life sciences. The technique has gained the most traction in neurobiology—the biology of the nervous system—where specific wavelengths of light are used to control or measure the activity of neurons in transgenic organisms (i.e., those with artificially inserted genes).

These optical recording and stimulation techniques are used in nervous system …

Nel Positively Regulates The Genesis Of Retinal Ganglion Cells By Promoting Their Differentiation And Survival During Development, Chizu Nakamoto, Soh-Leh Kuan, Amy Findlay, Elaine Durward, Zhufeng Ouyang, Masaru Nakamoto, Ewa Zakrewska, Takuma Endo

Biology Faculty Publications

For correct functioning of the nervous system, the appropriate number and complement of neuronal cell types must be produced during development. However, the molecular mechanisms that regulate the production of individual classes of neurons are poorly understood. In this study, we investigate the function of the thrombospondin-1–like glycoprotein, Nel (neural epidermal growth factor [EGF]-like), in the generation of retinal ganglion cells (RGCs) in chicks. During eye development, Nel is strongly expressed in the presumptive retinal pigment epithelium and RGCs. Nel overexpression in the developing retina by in ovo electroporation increases the number of RGCs, whereas the number of displaced amacrine …

Inducing Task-Relevant Responses To Speech In The Sleeping Brain, Sid Kouider, Thomas Andrillon, Leonardo S. Barbosa, Louise Goupil, Tristan A. Bekinschtein

Biology Faculty Publications

Falling asleep leads to a loss of sensory awareness and to the inability to interact with the environment [1]. While this was traditionally thought as a consequence of the brain shutting down to external inputs, it is now acknowledged that incoming stimuli can still be processed, at least to some extent, during sleep [2]. For instance, sleeping participants can create novel sensory associations between tones and odors [3] or reactivate existing semantic associations, as evidenced by event-related potentials [4; 5; 6 ; 7]. Yet, the extent to which the brain …

Brief Embryonic Strychnine Exposure In Zebrafish Causes Long-Term Adult Behavioral Impairment With Indications Of Embyronic Synaptic Changes, Nicole M. Roy, Brianna Arpie, Joseph Lugo, Elwood Linney, Edward D. Levin, Daniel Cerutti

Biology Faculty Publications

Zebrafish provide a powerful model of the impacts of embryonic toxicant exposure on neural development that may result in long-term behavioral dysfunction. In this study, zebrafish embryos were treated with 1.5mM strychnine for short embryonic time windows to induce transient changes in inhibitory neural signaling, and were subsequently raised in untreated water until adulthood. PCR analysis showed indications that strychnine exposure altered expression of some genes related to glycinergic, GABAergic and glutamatergic neuronal synapses during embryonic development. In adulthood, treated fish showed significant changes in swimming speed and tank diving behavior compared to controls. Taken together, these data show that …

Structure-Function Analysis Of Nel, A Thrombospondin-1-Like Glycoprotein Involved In Neural Development And Functions, Masaru Nakamoto

Biology Faculty Publications

Nel (neural epidermal growth factor (EGF)-like molecule) is a multimeric, multimodular extracellular glycoprotein with heparin-binding activity and structural similarities to thrombospondin-1. Nel is predominantly expressed in the nervous system and has been implicated in neuronal proliferation and differentiation, retinal axon guidance, synaptic functions, and spatial learning. The Nel protein contains an N-terminal thrombospondin-1 (TSP-N) domain, five cysteine-rich domains, and six EGF-like domains. However, little is known about the functions of specific domains of the Nel protein. In this study, we have performed structure-function analysis of Nel, by using a series of expression constructs for different regions of the Nel protein. …

Neural Coding Of Temporal Information And Its Topography In The Auditory Cortex, Thomas A. Terleph, Raphael Pinaud

Biology Faculty Publications

The article discusses a study that focused on neural coding of temporal information and topography in the auditory cortex. The quest for a thorough understanding how highly complex stimuli are encoded poses a significant challenge for auditory neurosciences, such as human speech and animal vocal signals. The characteristics of cortical neurons have been attributed to the coding of temporal stimulus which features precise spike timing in the coding and firing rate of repetition sounds.

Bilateral Multi-Electrode Neurophysiological Recordings Coupled To Local Pharmacology In Awake Songbirds, Liisa A. Tremere, Thomas A. Terleph, Jin Kwon Jeong, Raphael Pinaud

Biology Faculty Publications

Here we describe a protocol for bilateral multielectrode neurophysiological recordings during intracerebral pharmacological manipulations in awake songbirds. This protocol encompasses fitting adult animals with head-posts and recording chambers, and acclimating them to periods of restraint. The adaptation period is followed by bilateral penetrations of multiple electrodes to obtain acute, sensory-driven neurophysiological responses before versus during the application of pharmacological agents of interest. These local manipulations are achieved by simultaneous and restricted drug infusions carried out independently for each hemisphere. We have used this protocol to elucidate how neurotransmitter and neuroendocrine systems shape the auditory and perceptual processing of natural, learned …

In Vitro Guidance Of Retinal Axons By A Tectal Lamina-Specific Glycoprotein Nel, Yulan Jiang, Hiroya Obama, Soh-Leh Kuan, Ritsuko Nakamura, Chizu Nakamoto, Zhufeng Ouyang, Masaru Nakamoto

Biology Faculty Publications

Nel is a glycoprotein containing five chordin-like and six epidermal growth factor-like domains and is strongly expressed in the nervous system. In this study, we have examined expression patterns and in vitro functions of Nel in the chicken retinotectal system. We have found that in the developing tectum, expression of Nel is localized in specific laminae that retinal axons normally do not enter, including the border between the retinorecipient and non-retinorecipient laminae. Nel-binding activity is detected on retinal axons both in vivo and in vitro, suggesting that retinal axons express a receptor for Nel. In vitro, Nel inhibits retinal axon …

A Songbird Forebrain Area Potentially Involved In Auditory Discrimination And Memory Formation, Raphael Pinaud, Thomas A. Terleph

Biology Faculty Publications

Songbirds rely on auditory processing of natural communication signals for a number of social behaviors, including mate selection, individual recognition and the rare behavior of vocal learning - the ability to learn vocalizations through imitation of an adult model, rather than by instinct. Like mammals, songbirds possess a set of interconnected ascending and descending auditory brain pathways that process acoustic information and that are presumably involved in the perceptual processing of vocal communication signals. Most auditory areas studied to date are located in the caudomedial forebrain of the songbird and include the thalamo-recipient field L (subfields L1, L2 and L3), …

Neural Correlates Of Auditory Processing, Learning And Memory Formation In Songbirds, Raphael Pinaud, Thomas A. Terleph, Ryan D. Wynne, Liisa A. Tremere

Biology Faculty Publications

Songbirds have emerged as powerful experimental models for the study of auditory processing of complex natural communication signals. Intact hearing is necessary for several behaviors in developing and adult animals including vocal learning, territorial defense, mate selection and individual recognition. These behaviors are thought to require the processing, discrimination and memorization of songs. Although much is known about the brain circuits that participate in sensorimotor (auditory-vocal) integration, especially the “songcontrol” system, less is known about the anatomical and functional organization of central auditory pathways. Here we discuss findings associated with a telencephalic auditory area known as the caudomedial nidopallium (NCM). …