Biology subjects

Feldheim, D. A.

Publications and source records attributed to Feldheim, D. A..

6 recordsLinked to original sources

bioRxiv2026

Population decoding of sound source location by receptive field neurons in the mouse superior colliculus

Identifying the location of a sound source in a complex environment and assessing its importance can be crucial for survival. The superior colliculus (SC), a midbrain structure involved in sensorimotor functions, contributes to sound localization and contains auditory responsive neurons that have spatially restricted receptive fields (RFs) that are organized into a topographic map along the azimuth. However, individual auditory SC neurons have large spatial RFs, are noisy, and do not respond to the same stimulus at each trial. Therefore, when an animal is presented with a "single trial" sound, and it needs to rely on a single neuron to locate the sound source direction, the location measurement may be erroneous, missing, or have poor spatial resolution. It is expected that a more reliable and accurate determination of the sound source location will come from a population of neurons. We therefore built a population pattern Maximum Likelihood Estimation (MLE) decoder to build a model that can accurately predict the location of a stimulus given the population response. We compared three models that use either strict firing rate (FR), weighting based on equal (EW) or mutual information (MIW) and show that the MIW model works best, needing only 92 neurons to localize a stimulus with behaviorally relevant precision. Furthermore, by comparing the models fit using the responses from non-RF and RF auditory neurons, we show that only RF neurons contain the information needed to localize a sound source. These results are consistent with the hypothesis that the SC uses a population of RF neurons to determine sound source location. Author SummaryBeing able to tell where a sound is coming from and how important it is can be critical for survival. The superior colliculus, a midbrain region involved in orienting behaviors, contains neurons that respond best to sounds coming from specific locations. This suggests that the combined activity of many neurons in the SC is used to determine sound location from a single sound event. To test this idea, we modeled responses from mouse SC neurons while sounds were played from different positions in space, both along the elevation and horizon. A model that weighted the most informative neurons performed best in both directions needing only 92 neurons to localize a stimulus with behaviorally relevant precision along the azimuth. Comparing the models fit using the responses from non-RF and RF auditory neurons, we show that only RF neurons contain the information needed to localize a sound source Overall, our findings show that the SC can accurately locate sounds in both horizontal and vertical space using a population-based strategy, providing a simple and effective solution for rapid sound localization.

neuroscience↗

bioRxiv2025

Characterization of auditory responsive neurons in the mouse superior colliculus to naturalistic sounds

Locating the source of a specific sound in a complex environment and determining its saliency is critical for survival. The superior colliculus (SC), a sensorimotor midbrain structure, plays an important role in sound localization and has been shown to have a topographic map of the auditory space in a range of species. In mice, previous studies using broadband white noise stimuli found that neurons use high-frequency monaural spectral cues and interaural level differences (ILDs) to compute spatially restricted receptive fields (RFs), and that these RFs are organized topographically along the azimuth. However, in a naturalistic environment, the auditory stimuli that an animal encounters may have rich spectral components; however, these sound sources can still be localized efficiently. It remains unknown whether and how the SC neurons respond to naturalistic sounds and, in turn, compute a spatially restricted RF. Here, we show results from large-scale in vivo physiological recordings of SC neurons in response to white noise, naturalistic ultrasonic pup calls and chirps. We find that mouse SC auditory neurons respond to pup calls with distinct temporal patterns and a spatial preference predominantly at [~]60 degrees in contralateral azimuth. In addition, we categorized auditory SC neurons based on their spectrotemporal receptive field patterns and demonstrated that there are at least 4 distinct subtypes of auditory responsive SC neurons. Significance StatementThe superior colliculus (SC) receives visual and auditory information that is used to localize objects. While the organization and composition of visually responsive SC neurons is well described, much less is known about the types and response properties of auditory SC neurons. Here, we presented white noise, ultrasonic mouse pup calls, and chirp stimuli to mice while recording from SC neurons. Analysis of neuronal responses defines 4 distinct classes of auditory neurons. We also show that while auditory neurons respond to naturalistic stimuli, these responses mainly occur when presented from the side but not the front of the animal. These results lead to the hypothesis that mice use different strategies to localize sound depending on the spectral composition of the source.

neuroscience↗

bioRxiv2021

High-frequency hearing is required for generating a topographic map of auditory space in the mouse superior colliculus

A topographic map of auditory space is a feature found in the superior colliculus (SC) of many species, including CBA/CaJ mice. In this genetic background, high-frequency monaural spectral cues and interaural level differences are used to generate spatial receptive fields (RFs) that form a topographic map along the azimuth. Unfortunately, C57BL/6 mice, a strain widely used for transgenic manipulation, display age-related hearing loss (AHL) due to an inbred mutation in the Cadherin 23 gene (Cdh23) that affects hair cell mechanotransduction. To overcome this problem, researchers have used young C57BL/6 mice in their studies, as they have been shown to have normal hearing thresholds. However, important details of the auditory response characteristics of the SC such as spectral responses and spatial localization, have not been characterized in young C57BL/6 mice. Here we show that 2-4-month C57BL/6 mice lack neurons with frontal auditory RFs and therefore lack a topographic representation of auditory space in the SC. Analysis of the spectrotemporal receptive fields (STRFs) of the SC auditory neurons shows that C57BL/6 mouse SC neurons lack the ability to detect the high-frequency (>40kHz) spectral cues that are needed to compute frontal RFs. We also show that crossing C57BL/6 mice with CBA/CaJ mice or introducing one copy of the wild-type Cdh23 to C57BL/6 mice rescues the high-frequency hearing deficit and improves the topographic map of auditory space. Taken together, these results demonstrate the importance of high-frequency hearing in computing a topographic map of auditory space. Significance StatementDespite the strains age-dependent hearing loss, C57BL/6 mice are widely used in auditory studies because of the development of transgenic reporter and Cre lines in this genetic background. Here we examined the topographic map of auditory space and spectrotemporal properties of neurons in the SC of C57BL/6 mice. We found an early-onset high-frequency hearing deficit that results in the loss of SC neurons with frontal RFs and, consequently, an absence of a topographic map of auditory space. These findings stress the importance of high-frequency hearing in generating spatially restricted receptive fields and serve as a caution to researchers that doing auditory-related research using the C57BL/6 genetic background may not be representative of true wild-type mice.

neuroscience↗

bioRxiv2021

Nonlinear visuoauditory integration in the mouse superior colliculus

Sensory information from different modalities is processed in parallel, and then integrated in associative brain areas to improve object identification and the interpretation of sensory experiences. The Superior Colliculus (SC) is a midbrain structure that plays a critical role in integrating visual, auditory, and somatosensory input to assess saliency and promote action. Although the response properties of the individual SC neurons to visuoauditory stimuli have been characterized, little is known about the spatial and temporal dynamics of the integration at the population level. Here we recorded the response properties of SC neurons to spatially restricted visual and auditory stimuli using large-scale electrophysiology. We then created a general, population-level model that explains the spatial, temporal, and intensity requirements of stimuli needed for sensory integration. We found that the mouse SC contains topographically organized visual and auditory neurons that exhibit nonlinear multisensory integration. We show that nonlinear integration depends on properties of auditory but not visual stimuli. We also find that a heuristically derived nonlinear modulation function reveals conditions required for sensory integration that are consistent with previously proposed models of sensory integration such as spatial matching and the principle of inverse effectiveness.

neuroscience↗

bioRxiv2019

Spectral cues are necessary for encoding the azimuthal map of auditory space in the mouse superior colliculus

Sound localization plays a critical role in animal survival. Three cues can be used to compute sound direction: interaural timing differences (ITDs), interaural level differences (ILDs) and the direction-dependent spectral filtering by the head and pinnae (spectral cues). Little is known about how spectral cues contribute to the neural encoding of auditory space. Here we report on auditory space encoding in the mouse superior colliculus (SC). We show that the mouse SC contains neurons with spatially-restricted receptive fields (RFs) that form an azimuthal topographic map. We found that frontal RFs require spectral cues and lateral RFs require ILDs. The neurons with frontal RFs have frequency tunings that match the spectral structure of the specific head and pinna filter for sound coming from the front. These results demonstrate that patterned spectral cues in combination with ILDs give rise to the topographic map of azimuthal auditory space.

neuroscience↗

bioRxiv2016

Neurons in the mouse deep superior colliculus encode orientation/direction through suppression and extract selective visual features

The superior colliculus (SC) is an integrative sensorimotor structure that contributes to multiple visiondependent behaviors. It is a laminated structure; the superficial SC layers (sSC) contain cells that respond to visual stimuli, while the deep SC layers (dSC) contain cells that also respond to auditory and somatosensory stimuli. Despite the increasing interest in mice for visual system study, the differences in the visual response properties between the sSC and the dSC are largely unknown. Here we used a large-scale silicon probe recording system to examine the visual response properties of neurons within the SC of head-fixed, awake and behaving mice. We find that both the sSC and dSC cells respond to visual stimuli, but dSC cells have three key differences. (1) The majority of the dSC orientation/direction selective (OS/DS) cells have their firing rate suppressed by drifting sinusoidal gratings (negative OS/DS cells) rather than being stimulated like the sSC cells (positive OS/DS cells). (2) Almost all the dSC cells have complex-cell-like spatial summation nonlinearity, and a significantly smaller fraction of the positive OS/DS cells in the dSC respond to flashing spots than those in the sSC. (3) The dSC cells lack Y-like spatial summation nonlinearity unlike the sSC cells. These results provide the first description of cells that are suppressed by a visual stimulus with a specific orientation or direction, show that neurons in the dSC have properties analogous to cortical complex cells, and show the presence of Y-like nonlinearity in the sSC but their absence in the dSC.\n\nSignificance statementThe superior colliculus receives visual input from the retina in its superficial layers (sSC) and induces eye/head orientating movements and innate defensive responses in its deeper layers (dSC). Despite their importance, very little is known about the visual response properties of dSC neurons. Using highdensity electrode recordings and novel model-based analysis, we find that the dSC contains cells with a novel property; they are suppressed by the orientation or direction of specific stimuli. We also show that dSC cells have properties similar to cortical \"complex\" cells. Conversely, cells with Y-like nonlinear spatial summation properties are located only in the sSC. These findings contribute to our understanding of how the SC processes visual inputs, a critical step in comprehending visually-guided behaviors.\n\nAcknowledgementsThis work was supported by the Brain Research Seed Funding provided by UCSC and from the National Institutes of Health Grant NEI R21EYO26758 to D. A. F. and A. M. L. We thank Michael Stryker for training on the electrophysiology experiments and his very helpful comments on the manuscript, Sotiris Masmanidis for providing us with the silicon probes, Forest Martinez-McKinney and Serguei Kachiguin for their technical contributions to the silicon probe system, Jeremiah Tsyporin for taking an image of neural tissues and the training of mice, Jena Yamada, Anahit Hovhannisyan, Corinne Beier, and Sydney Weiser, for their helpful comments on the manuscript.

neuroscience↗