Dynamics of auditory cortical activity during behavioural engagement and auditory perception

Carcea, Ioana; Insanally, Michele N.; Froemke, Robert C.

doi:10.1038/ncomms14412

Cited by 91 publications

(118 citation statements)

References 55 publications

(86 reference statements)

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“…Immunohistochemistry was performed on the mounted sections as previously described (41,42). Sections were blocked in 5% goat serum solution for an hour at room temperature or for 14 hours at 4º C. A solution of the appropriate primary antibodies was diluted in 1% goat serum and 0.01% Triton X solution and then applied for 24 hours at 4º C. We used a…”

Section: Anatomymentioning

confidence: 99%

Oxytocin Neurons Enable Social Transmission of Maternal Behavior

Carcea

Caraballo

Marlin

et al. 2019

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Maternal care is profoundly important for mammalian survival, and maternal behaviors can also be expressed by non-biological parents after experience with infants. One critical molecular signal for maternal behavior is oxytocin, a hormone released in the brain by hypothalamic paraventricular nucleus (PVN). Oxytocin enables plasticity within the auditory cortex, a necessary step for responding to infant vocalizations. To determine how this change occurs during natural experience, we continuously monitored homecage behavior of female virgin mice co-housed for days with an experienced mother and litter, synchronized with in vivo recordings from virgin PVN cells, including from identified oxytocin neurons. Mothers engaged virgins in maternal care by ensuring that virgins were in the nest, and demonstrated maternal behavior in self-generated pup retrieval episodes. These social interactions activated virgin PVN and gated behaviorally-relevant cortical plasticity for pup distress calls. Thus rodent maternal behavior can be learned by social transmission, and our results describe a mechanism for adapting the brains of adult caregivers to infant needs via endogenous oxytocin. One Sentence Summary:Mother mice help co-housed virgins become maternal by enacting specific behaviors that activate virgin oxytocin neurons.Main Text: Social interactions, such as pair bond formation and child rearing, are fundamental aspects of animal and human behavior (1-4). Parental care is especially important in mammals, and new parents must rapidly and reliably express a number of behaviors required for survival of offspring. Some parental behavior is therefore believed to be at least in part innate and hard-wired, or gated by neurochemical changes after mating. However, maternal behavior can also be acquired from experience. In humans and other primates, individuals other than the biological parents can learn to successfully care for children after instruction or observation of experienced caretakers and infants (1-8). It is unclear how expression of such alloparenting behaviors in rodents or other species can also be learned from experience, and if so, what mechanisms of neuromodulation and plasticity underlie learning of maternal behaviors.One of the most important molecular modulators of neural circuit function for social interactions and maternal physiology is the evolutionarily-ancient peptide hormone oxytocin (1,2, 9,10). In mammals, oxytocin is released from the hypothalamus and is critical for childbirth and lactation (10,11). Oxytocin also acts in the brain where it is believed to increase the salience of social information, enhancing pair bonding and maternal behavior (1,9,(12)(13)(14)(15), and enabling onset of alloparenting in mice. Specifically, pup-naïve virgin female mice initially ignore neonates and cues related to infant need, e.g., ultrasonic distress calls emitted by pups isolated from the nest (15). However, after several days of co-housing with experienced mothers ('dams') and litters, most virgin females become mate...

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Section: Anatomymentioning

confidence: 99%

Oxytocin Neurons Enable Social Transmission of Maternal Behavior

Carcea

Caraballo

Marlin

et al. 2019

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“…We performed in vivo 2-photon imaging experiments in awake mice of C57 strain as well as CBA background (CBAxC57 F1) and quantified the functional responses across L2/3 and L4 of A1. We focused on young adult animals (~2-3 months old) which is the age frequently used in functional studies, especially those involving mouse behavior (Bandyopadhyay et al, 2010;Rothschild et al, 2010;Carcea et al, 2017;Guo et al, 2017;Kuchibhotla et al, 2017;Li et al, 2017;Meng et al, 2017;Resnik and Polley, 2017;Francis et al, 2018;Liu et al, 2019;Tischbirek et al, 2019). To compare strains we imaged the mid-frequency region of A1 (4-16kHz) which is also where mice are most sensitive to sound (Zheng et al, 1999).We find that A1 of CBA mice contains more neurons tuned to high frequencies and a higher number of significant tone-responses overall, including a higher proportion of off-responses (Liu et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Functional Organization of Mouse Primary Auditory Cortex in adult C57BL/6 and F1 (CBAxC57) mice

Bowen

Winkowski

2019

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The primary auditory cortex (A1) plays a key role for sound perception since it represents one of the first cortical processing stations for sounds. Recent studies have shown that on the cellular level the frequency organization of A1 is more heterogeneous than previously appreciated. However, many of these studies were performed in mice on the C57BL/6 background which develop high frequency hearing loss with age making them a less optimal choice for auditory research. In contrast, mice on the CBA background retain better hearing sensitivity in old age.Since potential strain differences could exist in A1 organization between strains, we performed comparative analysis of neuronal populations in A1 of adult (~10 weeks) C57BL/6 mice and CBAxC57 F1 mice. We used in vivo 2-photon imaging of pyramidal neurons in cortical layers L4 and L2/3 of awake mouse primary auditory cortex (A1) to characterize the populations of neurons that were active to tonal stimuli. Pure tones recruited neurons of widely ranging frequency preference in both layers and strains with neurons in CBA mice exhibiting a wider range of frequency preference particularly to higher frequencies. Frequency selectivity was slightly higher in C57BL/6 mice while neurons in CBA mice showed a greater sound-level sensitivity. The spatial heterogeneity of frequency preference was present in both strains with CBA mice exhibiting higher tuning diversity across all measured length scales. Our results demonstrate that the tone evoked responses and frequency representation in A1 of adult C57BL/6 and CBAxC57 F1 mice is largely similar.

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“…The attenuation of sound-evoked activity may decrease the sensitivity to sounds, as supported by poorer performance on tone detection tasks during locomotion (McGinley et al, 2015;). On the other hand, the observed increase in frequency selectivity in IC neurons may improve frequency discrimination (Aizenberg et al, 2015;Carcea et al, 2017;Guo et al, 2017).…”

Section: Modulation Of Neural Activity By Locomotion In the Icmentioning

confidence: 99%

Integration of locomotion and auditory signals in the mouse inferior colliculus

Yang

Lee

2019

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The inferior colliculus (IC) is the major midbrain auditory integration center, where virtually all ascending auditory inputs converge. Although the IC has been extensively studied for sound processing, little is known about the neural activity of the IC in moving subjects, as frequently happens in natural hearing conditions. Here we show, by recording the IC neural activity in walking mice, the activity of IC neurons is strongly modulated by locomotion in the absence of sound stimulus presentation. Similar modulation was also found in deafened mice, demonstrating that IC neurons receive non-auditory, locomotion-related neural signals.Sound-evoked activity was attenuated during locomotion, and the attenuation increased frequency selectivity across the population, while maintaining preferred frequencies. Our results suggest that during behavior, integrating movement-related and auditory information is an essential aspect of sound processing in the IC.The inferior colliculus (IC) is the major auditory integration center in the midbrain, where virtually all ascending inputs from the auditory brainstem and the descending cortical inputs converge (Adams, 1979(Adams, , 1980Malmierca, 2004;Winer and Schreiner, 2005). The IC plays a critical role in auditory processing, such as representing spectrotemporal features and communication sounds (Egorova et al.While auditory response properties have been extensively studied, most of neural recordings in the IC have been performed in stationary subjects, and little is known about the IC activity while subjects are engaged in locomotion.The central nucleus of the IC is considered a predominantly auditory structure. In contrast, the shell region of the IC (the lateral and dorsal cortex) receives non-auditory inputs such as somatosensory inputs (Cooper and Young, 1976;Morest and Oliver, 1984;Coleman and Clerici, 1987;Lesicko et al., 2016) and is thought to perform multi-sensory integration (Aitkin et al., 1978(Aitkin et al., , 1981 Jain and Shore, 2016). The shell region has also been implicated in generating sound-driven behavior by projecting to motor-related regions (Huffman and Henson, 1990;Xiong et al., 2015). Although this multi-modal integration may subserve a range of functions (Gruters and Groh, 2012), modulation of the IC activity during vocalization (Schuller, 1979;Tammer et al., 2004; ) or eye movements (Groh et al., 2001;Porter et al., 2006Porter et al., , 2007 suggests that a main role of the non-auditory inputs is providing motor-related information.Movement adds challenges to auditory processing such as recognizing sounds associated with movement itself or changing spatial relationships with a sound source. In order to Neural modulation precedes locomotion onsetWhen mice walk on a treadmill, the movements generate low intensity sounds. Therefore, NeurophysiologyMice were acclimated to head-fixing and walking on a passive disc-type treadmill for 2-4 days (one 30 min session per day) prior to neurophysiological recordings. On the day of significantly modulated by lo...

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Dynamics of auditory cortical activity during behavioural engagement and auditory perception

Cited by 91 publications

References 55 publications

Oxytocin Neurons Enable Social Transmission of Maternal Behavior

Oxytocin Neurons Enable Social Transmission of Maternal Behavior

Functional Organization of Mouse Primary Auditory Cortex in adult C57BL/6 and F1 (CBAxC57) mice

Integration of locomotion and auditory signals in the mouse inferior colliculus

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