Inhibitory Plasticity in a Lateral Band Improves Cortical Detection of Natural Vocalizations

Galindo-Leon, Edgar; Lin, Frank; Liu, Robert C.

doi:10.1016/j.neuron.2009.05.001

Cited by 118 publications

(158 citation statements)

References 42 publications

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“…Similarly, the frequency dependence of sweep direction selectivity was disrupted by pulsed noise exposure during P8 -P15 and P24 -P39. Because these response features are determined by multiple (e.g., excitatory and inhibitory) cortical circuits (Galindo-Leon et al 2009;Razak and Fuzessery 2009;Zhang et al 2003), our results are consistent with multiple sensitive periods for the development of these different circuits.…”

Section: Discussionsupporting

confidence: 79%

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Pulsed Noise Experience Disrupts Complex Sound Representations

Insanally

Albanna

Bao

2010

Journal of Neurophysiology

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Insanally MN, Albanna BF, Bao S. Pulsed noise experience disrupts complex sound representations. J Neurophysiol 103: 2611-2617, 2010. First published March 3, 2010 doi:10.1152/jn.00872.2009. Cortical sound representations are adapted to the acoustic environment. Early exposure to exponential frequency-modulated (FM) sweeps results in more neurons selective to the experienced sounds. Here we examined the influence of pulsed noise experience on the development of sound representations in the primary auditory cortex (AI) of the rat. In naïve animals, FM sweep direction selectivity depends on the characteristic frequency (CF) of the neuron-low CF neurons tend to select for upward sweeps and high CF neurons for downward sweeps. Such a CF dependence was not observed in animals that had received weeklong exposure to pulsed noise in periods from postnatal day 8 (P8) to P15 or from P24 to P39. In addition, AI tonotopicity, tuning bandwidth, intensity threshold, toneresponsiveness, and sweep response magnitude were differentially affected by the noise experience depending on the exposure time windows. These results are consistent with previous findings of feature-dependent multiple sensitive periods. The different effects induced here by pulsed noise and previously by FM sweeps further indicate that plasticity in cortical complex sound representations is specific to the sensory input. I N T R O D U C T I O NEarly experience has a significant influence on complex sound processing at both the behavioral and neuronal representational levels. Juvenile songbirds must hear tutor song early in life to accurately reproduce the learned song later in development (Marler and Peters 1982). Experience-dependent plasticity has been shown for the learning of the zebra finches' own song (Doupe and Solis 1997;Volman 1993).Electrophysiological studies show that neurons in the auditory forebrain of songbirds are selective for natural sounds (Grace et al. 2003;Margoliash 1986;Müller and Leppelsack 1985;Woolley et al. 2005), and such selectivity develops gradually (Amin et al. 2007). In addition to shaping perceptual behaviors, early experience also alters sensory neuronal representations (Brainard and Knudsen 1993;de Villers-Sidani et al. 2007Fagiolini et al. 1994;Han et al. 2007;Kim and Bao 2009;Merzenich et al. 1984;Polley et al. 2004;Simons and Land 1987;Takahashi et al. 2006; Van der Loos and Woolsey 1973;Wiesel and Hubel 1963;Zhang et al. 2001). In mammals, it has recently been shown that the maintenance and refinement of FM sweep selectivity are experience dependent (Razak et al. 2008). The development of complex sound features emerges in a series of sensitive periods within a monthlong critical period window. Early exposure to frequency-modulated (FM) sweeps alters frequency and bandwidth representations, and later exposure changes FM sweep selectivity (Insanally et al. 2009). This study did not, however, rule out the possibility that the observed effects were mainly caused by the broadband nature of the selected FM stimulus and not...

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Section: Discussionsupporting

confidence: 79%

“…Sweep direction selectivity is presumably mediated in part by sideband inhibition (Galindo-Leon et al 2009;Razak and Fuzessery 2009;Zhang et al 2003). Sideband inhibition for high-CF neurons is located mostly on the low frequency side, giving rise to its selectivity for downward sweeps.…”

Section: Discussionmentioning

confidence: 99%

Pulsed Noise Experience Disrupts Complex Sound Representations

Insanally

Albanna

Bao

2010

Journal of Neurophysiology

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“…A greater selectivity for frequency than timing cues for individual identification has also been seen in mice. Auditory cortex responses of mouse mothers carry more information about pup calls than those of virgins, primarily because of changes in frequency coding (Galindo-Leon et al 2009;Liu and Schreiner 2007).…”

Section: Discussionmentioning

confidence: 99%

Differential Influence of Frequency, Timing, and Intensity Cues in a Complex Acoustic Categorization Task

Nagel

McLendon

Doupe

2010

Journal of Neurophysiology

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Nagel KI, McLendon HM, Doupe AJ. Differential influence of frequency, timing, and intensity cues in a complex acoustic categorization task. J Neurophysiol 104: 1426 -1437, 2010. First published July 7, 2010 doi:10.1152/jn.00028.2010. Songbirds, which, like humans, learn complex vocalizations, provide an excellent model for the study of acoustic pattern recognition. Here we examined the role of three basic acoustic parameters in an ethologically relevant categorization task. Female zebra finches were first trained to classify songs as belonging to one of two males and then asked whether they could generalize this knowledge to songs systematically altered with respect to frequency, timing, or intensity. Birds' performance on song categorization fell off rapidly when songs were altered in frequency or intensity, but they generalized well to songs that were changed in duration by Ͼ25%. Birds were not deaf to timing changes, however; they detected these tempo alterations when asked to discriminate between the same song played back at two different speeds. In addition, when birds were retrained with songs at many intensities, they could correctly categorize songs over a wide range of volumes. Thus although they can detect all these cues, birds attend less to tempo than to frequency or intensity cues during song categorization. These results are unexpected for several reasons: zebra finches normally encounter a wide range of song volumes but most failed to generalize across volumes in this task; males produce only slight variations in tempo, but females generalized widely over changes in song duration; and all three acoustic parameters are critical for auditory neurons. Thus behavioral data place surprising constraints on the relationship between previous experience, behavioral task, neural responses, and perception. We discuss implications for models of auditory pattern recognition.

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“…Thus, taken together, the ECM influences short-and longterm plasticity of synapses and thereby potentially regulates signal processing within a neuronal network during learning. Indeed, auditory associative learning has been correlated with structural changes of topographic connections within primary ACx (19,(29)(30)(31), changes in interneuron activity (32,33), and Ca 2+ -dependent synaptic processing (34). However, further work will have to investigate the exact cellular and network effects of ECM removal in sensory cortex during learning processes in vivo.…”

Section: Potential Cellular Mechanisms Of Ecm-derived Modulation Ofmentioning

confidence: 99%

Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex

Happel

Niekisch²,

Rivera³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

150

118

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During brain maturation, the occurrence of the extracellular matrix (ECM) terminates juvenile plasticity by mediating structural stability. Interestingly, enzymatic removal of the ECM restores juvenile forms of plasticity, as for instance demonstrated by topographical reconnectivity in sensory pathways. However, to which degree the mature ECM is a compromise between stability and flexibility in the adult brain impacting synaptic plasticity as a fundamental basis for learning, lifelong memory formation, and higher cognitive functions is largely unknown. In this study, we removed the ECM in the auditory cortex of adult Mongolian gerbils during specific phases of cortex-dependent auditory relearning, which was induced by the contingency reversal of a frequency-modulated tone discrimination, a task requiring high behavioral flexibility. We found that ECM removal promoted a significant increase in relearning performance, without erasing already establishedthat is, learned-capacities when continuing discrimination training. The cognitive flexibility required for reversal learning of previously acquired behavioral habits, commonly understood to mainly rely on frontostriatal circuits, was enhanced by promoting synaptic plasticity via ECM removal within the sensory cortex. Our findings further suggest experimental modulation of the cortical ECM as a tool to open short-term windows of enhanced activitydependent reorganization allowing for guided neuroplasticity.chondroitin sulfate proteoglycan | hyaluronidase | perineuronal net | intracortical microinjection | strategy change S tructural remodeling and stabilization of synaptic networks are key mechanisms underlying learning in the adult brain. During early life, high structural and functional plasticity is required for the experience-shaped development of basic neuronal circuits (1). With brain maturation, juvenile plasticity of so-called critical or sensitive periods is decreased and is accompanied by the appearance of the brain's extracellular matrix (ECM) and its specialized compact form named "perineuronal net" (PNN) enwrappping cell bodies and synaptic contacts (2, 3). Enzymatic degradation of the ECM in adult animals has been demonstrated to restore such forms of developmental (juvenile) plasticity with respect to topographical map plasticity in the visual cortex (4), fearresponse-mediating circuits in the amygdala (5), spinal cord injuries (6, 7), and song learning circuits of zebra finches (8). In addition, enzymatic ECM removal altered several forms of synaptic plasticity in vitro and in vivo (9-12). However, even though structural stability of networks acquired during developmental phases is essential for neuronal efficiency, mechanisms allowing synaptic remodeling are key events during learning and memory formation throughout life (13). We recently demonstrated that endogenous proteases moderately digesting specific components of the ECM are regulated in an activity-dependent manner (2, 14) and ECM removal modulates synaptic short-term plasticity by synaptic e...

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Inhibitory Plasticity in a Lateral Band Improves Cortical Detection of Natural Vocalizations

Cited by 118 publications

References 42 publications

Pulsed Noise Experience Disrupts Complex Sound Representations

Pulsed Noise Experience Disrupts Complex Sound Representations

Differential Influence of Frequency, Timing, and Intensity Cues in a Complex Acoustic Categorization Task

Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex

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