Assistant Professor, Department of Biology
Research Interests: Neuronal circuits that mediate behavioral flexibility and attention; auditory coding; neural computation
Overview: We study the neural circuits that mediate auditory cognition. Our goal is to understand how we assign meaning to sounds, how we attend to sounds or ignore them, how we remember them, and how disorders of the brain can affect these processes.
Of particular interest is how our responses to sounds can change depending on context, a phenomenon called behavioral flexibility. Behaving appropriately after changes in context requires that organisms rapidly modify their expectations, associations between cues and rewards, or attentional state. Our lab investigates these cognitive processes by addressing three questions:
- What happens to the speed and accuracy of behavioral responses after a change in context?
- Where in the brain is information selected and re-routed to allow for different interpretations of the same stimulus?
- How do neural circuits implement this flexibility?
In our experiments, we use tools for monitoring and manipulating neuronal activity of specific cell types in behaving rodents, together with theoretical and computational approaches, to uncover the mechanisms that underlie flexible behaviors.
Auditory Thalamostriatal and Corticostriatal Pathways Convey Complementary Information about Sound Features.
J Neurosci. 2019 Jan 09;39(2):271-280
Authors: Ponvert ND, Jaramillo S
Multiple parallel neural pathways link sound-related signals to behavioral responses. For instance, the striatum, a brain structure involved in action selection and reward-related learning, receives neuronal projections from both the auditory thalamus and auditory cortex. It is not clear whether sound information that reaches the striatum through these two pathways is redundant or complementary. We used an optogenetic approach in awake mice of both sexes to identify thalamostriatal and corticostriatal neurons during extracellular recordings, and characterized neural responses evoked by sounds of different frequencies and amplitude modulation rates. We found that neurons in both pathways encode sound frequency with similar fidelity, but display different coding strategies for amplitude modulated noise. Whereas corticostriatal neurons provide a more accurate representation of amplitude modulation rate in their overall firing rate, thalamostriatal neurons convey information about the precise timing of acoustic events. These results demonstrate that auditory thalamus and auditory cortex neurons provide complementary information to the striatum, and suggest that these pathways could be differentially recruited depending on the requirements of a sound-driven behavior.SIGNIFICANCE STATEMENT Sensory signals from the cerebral cortex and the thalamus converge onto the striatum, a nucleus implicated in reward-related learning. It is not clear whether these two sensory inputs convey redundant or complementary information. By characterizing the sound-evoked responses of thalamostriatal and corticostriatal neurons, our work demonstrates that these neural pathways convey complementary information about the temporal features of sounds. This work opens new avenues for investigating how these pathways could be selectively recruited depending on task demands, and provides a framework for studying convergence of cortical and thalamic information onto the striatum in other sensory systems.
PMID: 30459227 [PubMed - in process]
The role of sensory cortex in behavioral flexibility.
Neuroscience. 2017 03 14;345:3-11
Authors: Guo L, Ponvert ND, Jaramillo S
To thrive in a changing environment, organisms evolved strategies for rapidly modifying their behavioral responses to sensory stimuli. In this review, we investigate the role of sensory cortical circuits in these flexible behaviors. First, we provide a framework for classifying tasks in which flexibility is required. We then present studies in animal models which demonstrate that responses of sensory cortical neurons depend on the expected outcome associated with a stimulus. Last, we discuss inactivation studies which indicate that sensory cortex facilitates behavioral flexibility, but is not always required for adapting to changes in environmental conditions. This analysis provides insights into the contributions of cortical and subcortical sensory circuits to flexibility in behavior.
PMID: 27066768 [PubMed - indexed for MEDLINE]
Adaptive categorization of sound frequency does not require the auditory cortex in rats.
J Neurophysiol. 2015 Aug;114(2):1137-45
Authors: Gimenez TL, Lorenc M, Jaramillo S
A defining feature of adaptive behavior is our ability to change the way we interpret sensory stimuli depending on context. Rapid adaptation in behavior has been attributed to frontal cortical circuits, but it is not clear if sensory cortexes also play an essential role in such tasks. In this study we tested whether the auditory cortex was necessary for rapid adaptation in the interpretation of sounds. We used a two-alternative choice sound-categorization task for rats in which the boundary that separated two acoustic categories changed several times within a behavioral session. These shifts in the boundary resulted in changes in the rewarded action for a subset of stimuli. We found that extensive lesions of the auditory cortex did not impair the ability of rats to switch between categorization contingencies and sound discrimination performance was minimally impaired. Similar results were obtained after reversible inactivation of the auditory cortex with muscimol. In contrast, lesions of the auditory thalamus largely impaired discrimination performance and, as a result, the ability to modify behavior across contingencies. Thalamic lesions did not impair performance of a visual discrimination task, indicating that the effects were specific to audition and not to motor preparation or execution. These results suggest that subcortical outputs of the auditory thalamus can mediate rapid adaptation in the interpretation of sounds.
PMID: 26156379 [PubMed - indexed for MEDLINE]
ErbB4 regulation of a thalamic reticular nucleus circuit for sensory selection.
Nat Neurosci. 2015 Jan;18(1):104-11
Authors: Ahrens S, Jaramillo S, Yu K, Ghosh S, Hwang GR, Paik R, Lai C, He M, Huang ZJ, Li B
Selective processing of behaviorally relevant sensory inputs against irrelevant ones is a fundamental cognitive function whose impairment has been implicated in major psychiatric disorders. It is known that the thalamic reticular nucleus (TRN) gates sensory information en route to the cortex, but the underlying mechanisms remain unclear. Here we show in mice that deficiency of the Erbb4 gene in somatostatin-expressing TRN neurons markedly alters behaviors that are dependent on sensory selection. Whereas the performance of the Erbb4-deficient mice in identifying targets from distractors was improved, their ability to switch attention between conflicting sensory cues was impaired. These behavioral changes were mediated by an enhanced cortical drive onto the TRN that promotes the TRN-mediated cortical feedback inhibition of thalamic neurons. Our results uncover a previously unknown role of ErbB4 in regulating cortico-TRN-thalamic circuit function. We propose that ErbB4 sets the sensitivity of the TRN to cortical inputs at levels that can support sensory selection while allowing behavioral flexibility.
PMID: 25501036 [PubMed - indexed for MEDLINE]
Mice and rats achieve similar levels of performance in an adaptive decision-making task.
Front Syst Neurosci. 2014;8:173
Authors: Jaramillo S, Zador AM
Two opposing constraints exist when choosing a model organism for studying the neural basis of adaptive decision-making: (1) experimental access and (2) behavioral complexity. Available molecular and genetic approaches for studying neural circuits in the mouse fulfill the first requirement. In contrast, it is still under debate if mice can perform cognitive tasks of sufficient complexity. Here we compare learning and performance of mice and rats, the preferred behavioral rodent model, during an acoustic flexible categorization two-alternative choice task. The task required animals to switch between two categorization definitions several times within a behavioral session. We found that both species achieved similarly high performance levels. On average, rats learned the task faster than mice, although some mice were as fast as the average rat. No major differences in subjective categorization boundaries or the speed of adaptation between the two species were found. Our results demonstrate that mice are an appropriate model for the study of the neural mechanisms underlying adaptive decision-making, and suggest they might be suitable for other cognitive tasks as well.
PMID: 25278849 [PubMed]
Auditory thalamus and auditory cortex are equally modulated by context during flexible categorization of sounds.
J Neurosci. 2014 Apr 09;34(15):5291-301
Authors: Jaramillo S, Borges K, Zador AM
In a dynamic world, animals must adapt rapidly to changes in the meaning of environmental cues. Such changes can influence the neural representation of sensory stimuli. Previous studies have shown that associating a stimulus with a reward or punishment can modulate neural activity in the auditory cortex (AC) and its thalamic input, the medial geniculate body (MGB). However, it is not known whether changes in stimulus-action associations alone can also modulate neural responses in these areas. We designed a categorization task for rats in which the boundary that separated low- from high-frequency sounds varied several times within a behavioral session, thus allowing us to manipulate the action associated with some sounds without changing the associated reward. We developed a computational model that accounted for the rats' performance and compared predictions from this model with sound-evoked responses from single neurons in AC and MGB in animals performing this task. We found that the responses of 15% of AC neurons and 16% of MGB neurons were modulated by changes in stimulus-action association and that the magnitude of the modulation was comparable between the two brain areas. Our results suggest that the AC and thalamus play only a limited role in mediating changes in associations between acoustic stimuli and behavioral responses.
PMID: 24719107 [PubMed - indexed for MEDLINE]
The auditory cortex mediates the perceptual effects of acoustic temporal expectation.
Nat Neurosci. 2011 Feb;14(2):246-51
Authors: Jaramillo S, Zador AM
When events occur at predictable instants, anticipation improves performance. Knowledge of event timing modulates motor circuits and thereby improves response speed. By contrast, the neuronal mechanisms that underlie changes in sensory perception resulting from expectation are not well understood. We developed a behavioral procedure for rats in which we manipulated expectations about sound timing. Valid expectations improved both the speed and the accuracy of the subjects' performance, indicating not only improved motor preparedness but also enhanced perception. Single-neuron recordings in primary auditory cortex showed enhanced representation of sounds during periods of heightened expectation. Furthermore, we found that activity in auditory cortex was causally linked to the performance of the task and that changes in the neuronal representation of sounds predicted performance on a trial-by-trial basis. Our results indicate that changes in neuronal representation as early as primary sensory cortex mediate the perceptual advantage conferred by temporal expectation.
PMID: 21170056 [PubMed - indexed for MEDLINE]
Optimal coding predicts attentional modulation of activity in neural systems.
Neural Comput. 2007 May;19(5):1295-312
Authors: Jaramillo S, Pearlmutter BA
Neuronal activity in response to a fixed stimulus has been shown to change as a function of attentional state, implying that the neural code also changes with attention. We propose an information-theoretic account of such modulation: that the nervous system adapts to optimally encode sensory stimuli while taking into account the changing relevance of different features. We show using computer simulation that such modulation emerges in a coding system informed about the uneven relevance of the input features. We present a simple feedforward model that learns a covert attention mechanism, given input patterns and coding fidelity requirements. After optimization, the system gains the ability to reorganize its computational resources (and coding strategy) depending on the incoming attentional signal, without the need of multiplicative interaction or explicit gating mechanisms between units. The modulation of activity for different attentional states matches that observed in a variety of selective attention experiments. This model predicts that the shape of the attentional modulation function can be strongly stimulus dependent. The general principle presented here accounts for attentional modulation of neural activity without relying on special-purpose architectural mechanisms dedicated to attention. This principle applies to different attentional goals, and its implications are relevant for all modalities in which attentional phenomena are observed.
PMID: 17381267 [PubMed - indexed for MEDLINE]