Jose L Pena Lab

Publications

Wang Y, Pena JL (2013) Direction selectivity mediated by adaptation in the owl's inferior colliculus. J. Neurosci. 33(49):19167-75. Pubmed 

Space specific neurons in the owl’s inferior colliculus are selective for motion direction. We found that preference for sounds moving toward frontal space increased with eccentricity in spatial tuning. This distribution was consistent with larger receptive-field asymmetry in neurons tuned to more peripheral auditory space. Directions that elicited larger response induced stronger forward suppression on the response at subsequent locations along the sound’s trajectory, thus making the response direction selective. The paper concluded that response adaptation and receptive-field shape could explain direction selectivity to acoustic motion and an orderly distribution of preferred direction.

Steinberg LJ, Fischer BJ, Pena JL (2013) Binaural gain modulation of spectrotemporal tuning in the ILD coding pathway. J. Neurosci. 33:11089 –11099. Pubmed 

Interaural level difference (ILD) is a critical cue for sound localization. ILD-detector neurons in the owl’s lateral lemniscus (LLDp), equivalent to the mammalian LSO, receive excitatory input from one side and inhibitory from the other. Here we examined the spectrotemporal tuning of both type of inputs and how they converge. We found that the firing of LLDp neurons is highly locked to the stimulus envelope. The inhibitory input, acting as a gain modulator, enhances the reliability of envelope coding in LLDp.

Wang Y, Shanbhag SJ, Fischer BJ, Peña JL (2012) Population-wide bias of surround suppression in auditory spatial receptive fields of the owl's midbrain. J Neurosci. 32(31):10470-8. Pubmed 

The owl’s midbrain contains a map of auditory space where the front is overrepresented. This paper reports a population-wide bias in the receptive fields of the neurons that constitute the map, such that lateral suppression from frontal space was always stronger. The findings could be predicted by a population of neurons with preferred directions overrepresenting frontal space and exerting lateral inhibition on each other. Thus, the uneven distribution of spatial tuning explained the topography of an emergent tuning property.

Fischer BJ, Steinberg LJ, Fontaine B, Brette R, Peña JL (2011) Effect of instantaneous frequency glides on interaural time difference processing by auditory coincidence detectors. Proc Natl Acad Sci USA 108(44):18138-43. Pubmed 

Here we investigated the spectrotemporal selectivity of monaural inputs in neurons that detect interaural time difference (ITD). We found that these inputs are matched not just for frequency but for frequency over time. A model based on cross-correlation showed that ITD tuning depends strongly on this selectivity. We further showed that this refinement could develop through spike timing-dependent plasticity. This paper offered an alternative to how ITD tuning could be regulated.

Steinberg LJ, Peña JL (2011) Difference in response reliability predicted by spectrotemporal tuning in the cochlear nuclei of barn owls. J Neurosci. 31(9):3234-42. Pubmed 

This study initiated a bottom-up approach to how the auditory system encodes stimulus identity. Envelope coding was compared in the two cochlear nuclei of the barn owl, nucleus angularis (NA) and nucleus magnocellularis (NM). We found that NA neurons, although unable to accurately encode stimulus phase, lock more strongly to the stimulus envelope than NM units. Further, we could relate the shape of the spectrotemporal receptive fields to this enhanced tuning. These findings suggest a dichotomy in envelope coding as early as at the first stage in the central auditory pathway.

Fischer BJ, Peña JL (2011) Owl's behavior and neural representation predicted by Bayesian inference. Nat Neurosci. 14(8):1061-6. Pubmed 

Owls systematically underestimate peripheral source directions. This paper reports that this behavior is predicted by a Bayesian model that emphasizes central directions. It is proposed that a bias in the neural coding of auditory space achieves high behavioral accuracy in the front at the cost of inducing errors in the periphery. This bias was consistent with the overrepresentation of frontal space observed in the map. This paper also reports that the properties of the map and its neurons allow for a simple population vector to approximate Bayesian inference.

Penzo MA, Peña JL (2011) Depolarization-induced suppression of spontaneous release in the avian midbrain. J Neurosci. 31(10):3602-9. Pubmed 

This study focused on the modulation of spontaneous neurotransmitter release by retrograde messengers in the chicken midbrain. Spontaneous neurotransmitter release has been considered synaptic ‘noise’. Recent work, however, suggested that these events could contribute to synaptic function. We found that somatic depolarization suppressed spontaneous synaptic release onto chicken midbrain neurons. These results indicated that these cells can specifically modulate spontaneous neurotransmitter release of its afferent inputs in a retrograde manner.

Fischer BJ, Anderson CH, Peña JL (2009) Multiplicative auditory spatial receptive fields created by a hierarchy of population codes. PLoS One. 4(11):e8015. Pubmed 

We built a model that accounted for the emergence of spatial tuning in the owl’s midbrain. The model combined spatial cues nonlinearly but linearly across frequency, as suggested by our intracellular studies. This model provided two advances:  First, it embraced the diversity of spiking responses demonstrated experimentally; second, it reconciled  multiplicative responses of spatial cues with the presence of linear frequency integration. 

Pérez ML, Shanbhag SJ, Peña JL (2009) Auditory spatial tuning at the crossroads of the midbrain and forebrain. J Neurophysiol. 102(3):1472-82. Pubmed 

This paper compared the spatial tuning in the midbrain and the auditory thalamus. Thalamic cells respond to a broader frequency range and their tuning to binaural cues varies more across frequency than in the midbrain. The frequency dependence was enhanced by the response to lower frequencies in the thalamus. Despite these differences, neurons in the thalamus could display spatial receptive fields as selective as in the midbrain, suggesting that spatial coding undergoes a change at the entryway to the forebrain.

Penzo MA, Peña JL (2009) Endocannabinoid-mediated long-term depression in the avian midbrain expressed presynaptically and postsynaptically. J Neurosci. 29(13):4131-9.  Pubmed 

An in vitro preparation of the chicken midbrain was developed to study synaptic plasticity in the avian auditory midbrain. We recorded neurons in the external part of the auditory torus (EX). We studied the connection between EX cells and inputs originating in the midbrain. Repetitive stimulation of these inputs induced LTD, a single-cell process mediated by endocannabinoids. Endocannabinoids both decreased release probability and reduced postsynaptic NMDA-receptor currents. This was the first report of eCB-dependent LTD in the auditory midbrain.

Wild JM, Kubke MF, Peña JL (2008) A pathway for predation in the brain of the barn owl (Tyto alba): projections of the gracile nucleus to the "claw area" of the rostral wulst via the dorsal thalamus. J. Comp. Neurol.  509:156-66. Pubmed 

With our colleagues from Auckland, New Zealand, we visited the owl’s somatosensory system. The Wulst of birds, is largely visual, but a relatively small rostral portion contains a representation of the contralateral claw. We investigated whether the input to this “claw area” arises from dorsal thalamic neurons that, in turn, receive their somatosensory input from the gracile nucleus.  Using retrograde and anterograde tracers we found a trisynaptic pathway from the body periphery to the telencephalic Wulst, via the dorsal thalamus. This pathway is likely involved in the barn owl’s predatory behavior. 

Fischer BJ, Christianson GB, Peña JL (2008) Cross-correlation in the auditory coincidence detectors of owls. J Neurosci. 28(32):8107-15. Pubmed 

Interaural time difference (ITD) plays a central role in sound localization.  Theory predicts that neurons that detect ITD behave as cross-correlators.  While cross-correlation-like properties have been reported, attempts to show that the shape of the ITD response function is determined by the spectral tuning of these neurons, a core prediction of cross-correlation, have been unsuccessful.  The paper demonstrates this relationship in neurons of the owl’s nucleus laminaris, using reverse correlation to estimate the inputs from each side.

Christianson GB, Peña JL (2007) Preservation of spectrotemporal tuning between the nucleus laminaris and the inferior colliculus of the barn owl. J Neurophysiol. 97(5):3544-53. Pubmed 

Neurons in the initial stages of the owl’s auditory pathway phase lock to frequencies ass high as 8 kHz. However, phase locking is rapidly abolished in a single-step transition. This paper reports that despite two stages of convergence and loss of phase information, the pathway preserves spectrotemporal information in envelope-locked responses. It is also evidence of simultaneous rate- and timing-based coding strategies representing multiple stimulus parameters.  

Christianson GB, Peña JL (2006) Noise reduction of coincidence detector output by the inferior colliculus of the barn owl. J Neurosci. 26(22):5948-54. Pubmed 

This article showed that the brainstem of the barn owl realizes a processing analogous to averaging. It showed that the signal-to-noise ratio in encoding of the interaural time difference (ITD) abruptly increases from the place where it is computed to the inferior colliculus (IC). The rate-ITD functions of IC neurons require as little as a single stimulus presentation to show coherent tuning. Average-like processes have been predicted by models of sound localization to remove noise. These data support those predictions and address a recurrent them in theoretical neuroscience.

Peña JL, Konishi M (2004) Robustness of multiplicative processes in auditory spatial tuning. J Neurosci. 24: 8907-8910. Pubmed 

Here we tested if neural multiplication was tolerant to changes in the amplitude of one input, as a mathematical multiplication should be. For this, we changed the correlation of sound between the ears, which modulates the amplitude of one of the two independent inputs to these cells. We found that the multiplication remained, as predicted by the mathematical operation.

Peña JL, Konishi M (2002) From postsynaptic potentials to spikes in the genesis of auditory spatial receptive fields. J Neurosci. 22: 5652-5658. Pubmed 

Comparison of subthreshold postsynaptic potentials and spiking output of space-specific neurons recorded intracellularly in vivo showed that subthreshold receptive fields were much larger than those measured in spikes. The main cause of these changes was the strategic location of the spiking threshold. In addition, the thresholds of the spikes at the beginning of a sound were lower than those of later sound-induced spikes and of spontaneous spikes due to dependence between the spiking threshold and the preceding change in membrane potential. This phenomenon could account for the sharpening of ITD selectivity from the beginning to end of the stimulus.

Peña JL, Konishi M (2001) Auditory spatial receptive fields created by multiplication. Science. 292(5515):249-52. Pubmed 

The space-specific neurons of the owl showed one of the cleanest examples of multiplication by systems of neurons. Multiplication is a powerful processing tool that, if implemented by the brain, would explain the emergence of neural combination selectivity. The owl’s auditory system computes interaural time (ITD) and level (ILD) differences to create a two dimensional map of auditory space. A multiplication of separate inputs tuned to ITD and ILD could account for the response of these neurons to ITD-ILD pairs. This finding lent support not just to models of sound localization but also to the use of multiplication to describe combination selectivity by neurons.

Peña JL, Viete S, Funabiki K, Saberi K, Konishi M (2001) Cochlear and neural delays for coincidence detection in owls. J Neurosci. 21: 9455-9459. Pubmed 

This paper tested predictions of two alternative models of ITD detection: one that takes into consideration differences in wave propagation along the cochlear basilar membrane (“stereausis theory”) and another one that uses neural delays (“Jeffress model”). We showed that for the owl there is no need to invoke mechanisms other than neural delays to explain the detection of ITD.

Peña JL, Konishi M (2000) Cellular mechanisms for resolving phase ambiguity in the owl's inferior colliculus. Proc. Nat. Acad. Sci. USA 97: 11787-11792. Pubmed 

Here we reported intracellular in vivo recordings in the owl’s inferior colliculus for the first time. We studied how frequencies converge onto these cells to resolve the ambiguity inherent to the periodic nature of sound. The paper reports a largely sublinear integration across frequency and a central role of spiking threshold in disambiguating the response.

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