The Emergence of Vocal Communication & Behavior
The most influential contemporary neuroscience discoveries commonly depend on well-controlled, trial-based measures. However, these paradigm are not ideal for studying the maturation of behavior which occurs over weeks to years (in humans). Our current research uses continuous audio and video recordings from gerbil families to describe maturational events that cannot be studied with short-term observations. Using this approach, we discovered that gerbils display a rich vocal repertoire with family-specific usage patterns (Peterson et al., 2024a). In collaboration with the Williams and Schneider labs, we are developing a machine learning approach to localize and attribute vocalizations to individual animals within a social group (Peterson et al., 2024b). In collaboration with the Pereira lab, we are tracking each member of a gerbil family to reveal how early and sustained social interactions may support solitary exploration (Mitelut et al., 2025). We are now developing a large-scale living environment with an underground burrow system in which to study social vocal communication across weeks to months.
The Maturation of Auditory Perception and Learning
There is one class of beneficial experiences that is common to most developing mammals. Sensory and motor skills improve through practice. Virtually every human skill, from walking to aural communication, emerges slowly during development (Sanes & Wolley, 2011). Thus, our lab studies the neural mechanisms that support the emergence of adult perceptual (Sarro & Sanes, 2010, 2011; Sarro et al. 2015) and cognitive skills (Caras & Sanes, 2017; Yao & Sanes, 2020).
To explore the neural mechanisms that underpin the maturation of perception and perceptual learning (Caras & Sanes, 2019), we record wirelessly from auditory cortex while animals practice, and improve on, auditory psychometric tasks.
We are also exploring whether gerbils can learn from one another. In fact, our recent work suggests that auditory learning is facilitated by watching a littermate perform the task (Paraouty et al., 2020; Paraouty et al., 2021). Auditory cortex activity is necessary for this form of learning, and social exposure induced an improvement in auditory corterx neuron sensitivity to the task cues (Paraouty et al., 2023).
To explore the neural mechanisms that underpin the maturation of perception and perceptual learning (Caras & Sanes, 2019), we record wirelessly from auditory cortex while animals practice, and improve on, auditory psychometric tasks.
We are also exploring whether gerbils can learn from one another. In fact, our recent work suggests that auditory learning is facilitated by watching a littermate perform the task (Paraouty et al., 2020; Paraouty et al., 2021). Auditory cortex activity is necessary for this form of learning, and social exposure induced an improvement in auditory corterx neuron sensitivity to the task cues (Paraouty et al., 2023).
Early Hearing Loss Impairs Auditory Processing
At the other extreme, we study how diminished developmental experience, such as a brief period of hearing loss, can impair both sensory processing and skill learning (Buran et al. 2014; Caras & Sanes, 2015; Ihlefeld et al. 2016). For example, animals reared with conductive hearing loss display delayed learning on an amplitude modulation discrimination, and poorer psychometric thresholds (von Trapp et al. 2016). Recently, we have found that transient hearing loss occurring after the developmental critical period, but during adolescence, can also degrade auditory perception, although the changes induced in auditory cortex are quite distinct (Anbuhl et al., 2022).
By recording wirelessly from auditory cortex as animals perform an amplitude modulation depth detection task, we discovered that hearing loss leads to degraded encoding in auditory cortex neurons (i.e., a sensory deficit: Anbuhl et al., 2022), and diminished gain that ordinarily accompanies attention to the task (i.e., a cognitive deficit: Yao & Sanes, 2018). A similar effect is observed during amplitude modulation rate discrimination (Yao & Sanes, ARO 2019 Poster). These findings suggest that developmental hearing can induce deficits in both sensory and cognitive processing areas. At the other extreme, we study how diminished developmental experience, such as a brief period of hearing loss, can impair both sensory processing and skill learning (Buran et al. 2014; Caras & Sanes, 2015; Ihlefeld et al. 2016). For example, animals reared with conductive hearing loss display delayed learning on an amplitude modulation discrimination task, and poorer psychometric thresholds (von Trapp et al. 2017).
By recording wirelessly from auditory cortex as animals perform an amplitude modulation depth detection task, we discovered that hearing loss leads to degraded encoding in auditory cortex neurons (i.e., a sensory deficit: Anbuhl et al., 2022), and diminished gain that ordinarily accompanies attention to the task (i.e., a cognitive deficit: Yao & Sanes, 2018). A similar effect is observed during amplitude modulation rate discrimination (Yao & Sanes, ARO 2019 Poster). These findings suggest that developmental hearing can induce deficits in both sensory and cognitive processing areas. At the other extreme, we study how diminished developmental experience, such as a brief period of hearing loss, can impair both sensory processing and skill learning (Buran et al. 2014; Caras & Sanes, 2015; Ihlefeld et al. 2016). For example, animals reared with conductive hearing loss display delayed learning on an amplitude modulation discrimination task, and poorer psychometric thresholds (von Trapp et al. 2017).
Synaptic Properties that Support Auditory Perception
One general idea is that these behavioral deficits are due, in part, to the permanent changes to synapse function in specific areas of the brain, including auditory cortex. These synaptic deficits can be induced by even a temporary period of hearing loss (Mowery et al. 2015, 2016, 2017), such as occurs in children with chronic middle ear infections. Thus, a primary translational goal of our research is to understand how these cellular properties can be rescued, thereby restoring normal perceptual abilities.
To ask whether hearing loss-induced changes to auditory cortex cellular properties contribute to perceptual deficits, we have explored the effect of rescuing synaptic inhibition. These studies indicate that normal perceptual skills are restored when animals are treated with a GABAergic enhancer during the critical period (Mowery, Caras, et al., 2019). Our unpublished work suggests that GABAB receptor-mediated inhibition is particularly important for normal perception: virally-mediated expression of the Gabbr1b subunit in auditory cortex pyramidal neurons can restore perceptual performance on both amplitude and spectral modulation detection tasks (Masri et al., 2024).
To ask whether hearing loss-induced changes to auditory cortex cellular properties contribute to perceptual deficits, we have explored the effect of rescuing synaptic inhibition. These studies indicate that normal perceptual skills are restored when animals are treated with a GABAergic enhancer during the critical period (Mowery, Caras, et al., 2019). Our unpublished work suggests that GABAB receptor-mediated inhibition is particularly important for normal perception: virally-mediated expression of the Gabbr1b subunit in auditory cortex pyramidal neurons can restore perceptual performance on both amplitude and spectral modulation detection tasks (Masri et al., 2024).
Cortical Processing, Perception, & Cognitive Skills
A primary goal of systems neuroscience is to understand the neural basis of perceptual and cognitive skills. We routinely record from auditory cortex while animals perform psychometric tasks, and have discovered that spontaneous discharge is transiently reduced at the moment animals initiate a trial (Buran et al., 2014), and explored how cortical response variance declines during task performance (von Trapp et al., 2016). Our most recent work suggests that auditory cortex neurons over-represent the rising phase of slow amplitude modulated stimuli, including speech. This imparts a decoding benefit: a classifier can discriminate vocoded speech stimuli using summed population activity (Penikis & Sanes, 2023).
We have also explored how cortical population activity can account for envelope discrimination versus categorization (Yao & Sanes, 2021), and have extended our analysis - using a single interval alternative forced choice procedure - to parietal cortex, a region downstream of auditory cortex that mediates auditory decision-making (Yao et al., 2020). While parietal neurons represent behaviorally relevant auditory information when animals listen passively to these stimuli, it is only during task engagement that decoded parietal cortex activity directly reflects psychometric performance and behavioral measures of integration time (Yao et al., 2023). Furthermore, an animal's performance under difficult listening conditions depends on a top-down projection from cingulate to auditory cortex (Anbuhl et al., 2025). When the cingulate projection is inactivated, perceptual performance is degraded for hard, but not easy, tasks.
We have also explored how cortical population activity can account for envelope discrimination versus categorization (Yao & Sanes, 2021), and have extended our analysis - using a single interval alternative forced choice procedure - to parietal cortex, a region downstream of auditory cortex that mediates auditory decision-making (Yao et al., 2020). While parietal neurons represent behaviorally relevant auditory information when animals listen passively to these stimuli, it is only during task engagement that decoded parietal cortex activity directly reflects psychometric performance and behavioral measures of integration time (Yao et al., 2023). Furthermore, an animal's performance under difficult listening conditions depends on a top-down projection from cingulate to auditory cortex (Anbuhl et al., 2025). When the cingulate projection is inactivated, perceptual performance is degraded for hard, but not easy, tasks.
Drudgery-Associated Sound Attenuation Booth Assembly