A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks

Hurley, Laura M.; Devilbiss, DM; Bd, Waterhouse

doi:10.1016/j.conb.2004.06.007

Cited by 192 publications

(184 citation statements)

References 79 publications

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“…Because the current peri-LC BET and AMPA infusion parameters reliably increase tonic LC firing (Berridge and Foote, 1991) and disrupt PPI, whereas clonidine reduces tonic LC firing (Berridge et al, 1993) and normalizes BET-induced PPI deficits, the present results provide the first clear evidence for this hypothesis. LC-NE is also well known to regulate sensory signal processing, with enhanced NE transmission having the ability to improve signal-to-noise characteristics of sensory receptive fields in a number of modalities and sites Waterhouse, 2004, 2011;Escanilla et al, 2010;Hirata et al, 2006;Hurley et al, 2004;Moxon et al, 2007). LC-NE effects on sensory signal processing also seem to follow an inverted-U-shaped profile, raising the intriguing possibility that high levels of tonic LC-NE activation (as would be achieved with the pharmacological approaches of the present studies) might affect the processing of the prepulse in primary sensory pathways as that information is conveyed to the pontine nuclei that ultimately mediate PPI.…”

Section: Discussionmentioning

confidence: 99%

Pharmacological Stimulation of Locus Coeruleus Reveals a New Antipsychotic-Responsive Pathway for Deficient Sensorimotor Gating

Alsene

Bakshi

2011

Neuropsychopharmacol

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Surprisingly little is known about the modulation of core endophenotypes of psychiatric disease by discrete noradrenergic (NE) circuits. Prepulse inhibition (PPI), the diminution of startle responses when weak prestimuli precede the startling event, is a widely validated translational paradigm for information-processing deficits observed in several mental disorders including schizophrenia, Tourette's syndrome, and post-traumatic stress disorder (PTSD). Despite putative NE disturbances in these illnesses, NE regulation of PPI remains poorly understood. In these studies, regulation of PPI by the locus coeruleus (LC), the primary source of NE to forebrain, was evaluated in rats using well-established protocols to pharmacologically activate/inactivate this nucleus. The ability of drugs that treat deficient PPI in these illnesses to reverse LC-mediated PPI deficits was also tested. Stimulation of LC receptors produced an anatomically and behaviorally specific deficit in PPI that was blocked by clonidine (Cataprese, an a2 receptor agonist that reduces LC neuronal firing after peri-LC delivery), a postsynaptic a1 NE receptor antagonist (prazosin), and second-generation antipsychotics (olanzapine, seroquel), but not by drugs that antagonized dopamine-1 (SCH23390), dopamine-2 (the first-generation antipsychotic Haloperidol), or serotonin-2 receptors (ritanserin). These results indicate a novel substrate in the regulation of PPI and reveal a novel functional role for the LC. Hence, a hyperactive LC-NE system might underlie a deficient sensorimotor gating endophenotype in a subset of patients suffering from psychiatric illnesses including schizophrenia, Tourette's syndrome, and PTSD, and the ability to normalize LC-NE transmission could contribute to the clinical efficacy of certain drugs (Cataprese, prazosin, and second-generation antipsychotics) in these conditions.

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Section: Discussionmentioning

confidence: 99%

Pharmacological Stimulation of Locus Coeruleus Reveals a New Antipsychotic-Responsive Pathway for Deficient Sensorimotor Gating

Alsene

Bakshi

2011

Neuropsychopharmacol

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“…Indeed, many of the cortical targets of reward signals-such as oculomotor neurons in frontal and parietal cortex-are ideally situated to send modulatory feedback signals to earlier sensory areas so that the cortical representation of high-value stimulus features can be enhanced (Bisley and Goldberg 2003;Ding and Hikosaka 2006;Gold and Shadlen 2007;Serences and Yantis 2006;Shadlen and Newsome 2001). In addition to DA neurons, the locus ceruleus sends long-range norepinephrine projections that have been implicated in modulating activity in sensory cortices in response to highly relevant stimuli (Aston-Jones and Cohen 2005;Berridge 2008;Berridge and Waterhouse 2003;Hurley et al 2004;Manunta and Edeline 2004;Sara 2009;Schultz and Dickinson 2000). Thus although both DA and norepinephrine pathways are viable candidates for the induction of value-related modulations in early visual cortex, future research will be required to more precisely characterize the source of these modulations, perhaps using pharmacological interventions in combination with fMRI (e.g., Pleger et al 2009;Silver et al 2008).…”

Section: Value and Population Responses In Human Visual Cortexmentioning

confidence: 99%

Population Response Profiles in Early Visual Cortex Are Biased in Favor of More Valuable Stimuli

Serences

Saproo

2010

Journal of Neurophysiology

104

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Serences JT, Saproo S. Population response profiles in early visual cortex are biased in favor of more valuable stimuli. J Neurophysiol 104: 76 -87, 2010. First published April 21, 2010 doi:10.1152/jn.01090.2009. Voluntary and stimulus-driven shifts of attention can modulate the representation of behaviorally relevant stimuli in early areas of visual cortex. In turn, attended items are processed faster and more accurately, facilitating the selection of appropriate behavioral responses. Information processing is also strongly influenced by past experience and recent studies indicate that the learned value of a stimulus can influence relatively late stages of decision making such as the process of selecting a motor response. However, the learned value of a stimulus can also influence the magnitude of cortical responses in early sensory areas such as V1 and S1. These early effects of stimulus value are presumed to improve the quality of sensory representations; however, the nature of these modulations is not clear. They could reflect nonspecific changes in response amplitude associated with changes in general arousal or they could reflect a bias in population responses so that high-value features are represented more robustly. To examine this issue, subjects performed a two-alternative forced choice paradigm with a variableinterval payoff schedule to dynamically manipulate the relative value of two stimuli defined by their orientation (one was rotated clockwise from vertical, the other counterclockwise). Activation levels in visual cortex were monitored using functional MRI and feature-selective voxel tuning functions while subjects performed the behavioral task. The results suggest that value not only modulates the relative amplitude of responses in early areas of human visual cortex, but also sharpens the response profile across the populations of feature-selective neurons that encode the critical stimulus feature (orientation). Moreover, changes in space-or feature-based attention cannot easily explain the results because representations of both the selected and the unselected stimuli underwent a similar feature-selective modulation. This sharpening in the population response profile could theoretically improve the probability of correctly discriminating high-value stimuli from low-value alternatives.

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“…These serotonergic neurons, found mostly within the dorsal and median raphe nuclei, have their highest levels of activity in awake and alert animals but are less active in sleeping or inattentive animals (Trulson and Jacobs, 1979;Heym et al, 1982;Trulson and Trulson, 1982;Waterhouse et al, 2004). There is corresponding evidence across multiple sensory systems that serotonin alters sensory circuitry in highly selective ways that promote the extraction of features of sensory stimuli (for review, see Hurley et al, 2004).…”

Section: Functional Consequencesmentioning

confidence: 99%

“…However, despite this evidence, there has been little focus within the auditory system or other sensory systems on the specific ways that neuromodulators change latencies and whether these vary for different cell types or occur independently from neuromodulatory effects on response strength. In the experiments described here, we addressed these issues by applying serotonin iontophoretically while recording from single neurons in the inferior colliculus (IC), a nucleus in which the stimulus features that influence latency Fuzessery and Hall, 1996;Barsz et al, 1998;Klug et al, 2000;Galazyuk and Feng, 2001;Faure et al, 2003) and the modulation of response properties by serotonin Pollak, 1999, 2001;Hurley et al, 2002Hurley et al, , 2004 have been well studied. With this approach, we characterized serotonergic effects on latency by (1) quantifying serotonergic effects on the latency and precision of spikes, (2) comparing serotoninevoked changes in latency with changes in spike count and other response properties, and (3) determining the dependence of serotonin-evoked latency shifts on features of the stimulus.…”

Section: Introductionmentioning

confidence: 99%

Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons

Hurley¹,

Pollak²

2005

J. Neurosci.

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Many studies of neuromodulators have focused on changes in the magnitudes of neural responses, but fewer studies have examined neuromodulator effects on response latency. Across sensory systems, response latency is important for encoding not only the temporal structure but also the identity of stimuli. In the auditory system, latency is a fundamental response property that varies with many features of sound, including intensity, frequency, and duration. To determine the extent of neuromodulatory regulation of latency within the inferior colliculus (IC), a midbrain auditory nexus, the effects of iontophoretically applied serotonin on first-spike latencies were characterized in the IC of the Mexican free-tailed bat. Serotonin significantly altered the first-spike latencies in response to tones in 24% of IC neurons, usually increasing, but sometimes decreasing, latency. Serotonin-evoked changes in latency and spike count were not always correlated but sometimes occurred independently within individual neurons. Furthermore, in some neurons, the size of serotonin-evoked latency shifts depended on the frequency or intensity of the stimulus, as reported previously for serotonin-evoked changes in spike count. These results support the general conclusion that changes in latency are an important part of the neuromodulatory repertoire of serotonin within the auditory system and show that serotonin can change latency either in conjunction with broad changes in other aspects of neuronal excitability or in highly specific ways.

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A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks

Cited by 192 publications

References 79 publications

Pharmacological Stimulation of Locus Coeruleus Reveals a New Antipsychotic-Responsive Pathway for Deficient Sensorimotor Gating

Pharmacological Stimulation of Locus Coeruleus Reveals a New Antipsychotic-Responsive Pathway for Deficient Sensorimotor Gating

Population Response Profiles in Early Visual Cortex Are Biased in Favor of More Valuable Stimuli

Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons

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