Metabolic Effects of Blocking Tone Conditioning on the Rat Auditory System

Poremba, Amy; Jones, Dirk; González-Lima, Francisco

doi:10.1006/nlme.1997.3792

Cited by 27 publications

(27 citation statements)

References 43 publications

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“…As the neuronal energy demand to process and consolidate learned associations changes, so does the production of the CO enzyme (Wong-Riley, 1989, Gonzalez-Lima, 1992. Earlier findings from our laboratory have demonstrated that auditory fear conditioning in rats results in metabolic capacity changes in the auditory system, confirming that mapping CO metabolic activity using quantitative histochemistry can be used to examine sustained metabolic effects of behavioral training on the brain (Poremba et al, 1997, Poremba et al, 1998a, Poremba et al, 1998b. Another recent study found that several days of the excitatory tone-footshock conditioning in rats changed CO activity in septohippocampal areas (Conejo et al, 2005).…”

Section: Introductionsupporting

confidence: 55%

“…Cytochrome oxidase (CO) metabolic brain mapping provides an alternative approach for investigating neural circuits mediating Pavlovian conditioning, and it is a well-suited method for quantifying more stable neuronal metabolic capacity changes that reflect prolonged training (Poremba et al, 1997, Poremba et al, 1998b, Poremba et al, 1998a, Sakata et al, 2000, Villarreal et al, 2002, Conejo et al, 2005, Sakata et al, 2005. CO changes in the brain after prolonged training reach a more stabilized state of oxidative metabolism, and techniques which measure evoked brain metabolic activity, such as fluorodeoxyglucose (FDG) autoradiography, positron emission tomography (PET) or functional magnetic resonance imaging (fMRI) may not reflect sustained changes in baseline metabolic capacity (Gonzalez-Lima and Cada, 1998).…”

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Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning

Bruchey

González-Lima

2008

Neuroscience

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While Pavlovian conditioning alters stimulus-evoked metabolic activity in the cerebral cortex, less is known about the effects of Pavlovian conditioning on neuronal metabolic capacity. Pavlovian conditioning may increase prefrontal cortical metabolic capacity, as suggested by evidence of changes in cortical synaptic strengths, and evidence for a shift in memory initially processed in subcortical regions to more distributed prefrontal cortical circuits. Quantitative cytochrome oxidase histochemistry was used to measure cumulative changes in brain metabolic capacity associated with both cued and contextual Pavlovian conditioning in rats. The cued conditioned group received tonefootshock pairings to elicit a conditioned freezing response to the tone conditioned stimulus, while the contextually conditioned group received pseudorandom tone-footshock pairings in an excitatory context. Untrained control group was handled daily, but did not receive any tone presentations or footshocks. The cued conditioned group had higher cytochrome oxidase activity in the infralimbic and anterior cingulate cortex, and lower cytochrome oxidase activity in dorsal hippocampus than the other two groups. A significant increase in cytochrome oxidase activity was found in anterior cortical areas (medial, dorsal and lateral frontal cortex; agranular insular cortex; lateral and medial orbital cortex and prelimbic cortex) in both conditioned groups, as compared to the untrained control group. In addition, no differences in cytochrome oxidase activity in the somatosensory regions and the amygdala were detected among all groups. The findings indicate that cued and contextual Pavlovian conditioning induces sustained increases in frontal cortical neuronal metabolic demand resulting in regional enhancement in the metabolic capacity of anterior cortical regions. Enhanced metabolic capacity of these anterior cortical areas after Pavlovian conditioning suggests that the frontal cortex may play a role in the retention and regulation of learned associations. KeywordsCytochrome oxidase; hippocampus; amygdala; context Cytochrome oxidase (CO) metabolic brain mapping provides an alternative approach for investigating neural circuits mediating Pavlovian conditioning, and it is a well-suited method for quantifying more stable neuronal metabolic capacity changes that reflect prolonged training (Poremba et al., 1997, Poremba et al., 1998b, Poremba et al., 1998a, Sakata et al., 2000, Villarreal et al., 2002, Conejo et al., 2005, Sakata et al., 2005. CO changes in the brain after prolonged training reach a more stabilized state of oxidative metabolism, and techniques which measure evoked brain metabolic activity, such as fluorodeoxyglucose (FDG) autoradiography, Corresponding author: F. Gonzalez-Lima, Dept. of Psychology, 1 University Station A8000, University of Texas at Austin, Austin, TX 78712-0187, Telephone: 512 471-5895, Fax: 512 471-4728, E-mail: Gonzalez-lima@mail.utexas.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that...

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confidence: 55%

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Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning

Bruchey

González-Lima

2008

Neuroscience

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“…Using cytochrome oxidase as a metabolic marker, it has been demonstrated that secondary auditory cortex responds to an auditory conditioned stimulus predictive of footshock, but not if the stimulus is blocked by previous conditioning to a visual stimulus (Poremba et al, 1997). Metabolic differences between the two conditions were observed in structures in which the convergence of auditory and somatosensory input is modulated by visual input.…”

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Thalamic Reticular Nucleus Activation Reflects Attentional Gating during Classical Conditioning

2000

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All senses, except olfaction, are routed through the thalamus to cerebral cortex. Thus, the thalamus is often referred to as the sensory gateway to cortex. Located between thalamus and cortex is a thin lamina of neurons called the thalamic reticular nucleus, which may function as an attentional gate. The phenomenon of blocking in classical conditioning provides an opportunity to test whether an attended stimulus activates the thalamic reticular nucleus more than an unattended stimulus: when a second stimulus is presented together with a previously conditioned stimulus, conditioned responding to the second stimulus is inhibited.Different groups of rats were given conditioning sessions with a single stimulus, a light or a tone, and then given conditioning sessions with compound (light and tone) stimuli. Blocking was confirmed using probe trials of single stimulus presentations. After a final test session of compound stimulus presentations, the brains were processed for the presence of Fos protein. Here we show that Fos-positive neurons were more numerous in the sector of the thalamic reticular nucleus associated with the attended conditioned stimulus than in the sector associated with the unattended stimulus. Thus, we provide evidence for an involvement of the thalamic reticular nucleus in selective attention.

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“…A PubMed search of learning and memory studies using CO measures revealed over 75 studies, many of which have been reviewed recently by us and others (Sakata et al, 2005;Hu et al, 2006;Conejo et al, 2007). In particular, CO has been used successfully to detect subtle differences in regional brain metabolic capacity in behavioral learning tasks such as Pavlovian conditioning of tones and shocks (Poremba et al, 1997(Poremba et al, , 1998Conejo et al, 2005).Brain circuits related to learning have been often investigated by measuring the activity of specific neural regions. Schmajuk et al (1996); et al, 2000).…”

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Functional networks underlying latent inhibition learning in the mouse brain

et al. 2007

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The present study reports the first comprehensive map of brain networks underlying latent inhibition learning and the first application of structural equation modeling to cytochrome oxidase data. In latent inhibition, repeated exposure to a stimulus results in a latent form of learning that inhibits subsequent associations with that stimulus. As neuronal energy demand to form learned associations changes, so does the induction of the respiratory enzyme cytochrome oxidase. Therefore, cytochrome oxidase can be used as an endpoint metabolic marker of the effects of experience on regional brain metabolic capacity. Quantitative cytochrome oxidase histochemistry was used to map brain regions in mice trained on a tone-footshock fear conditioning paradigm with either tone preexposure (latent inhibition), conditioning only (acquisition), conditioning followed by tone alone (extinction), or no handling or conditioning (naïve). The ventral cochlear nucleus, medial geniculate, CA1 hippocampus, and perirhinal cortex showed modified metabolic capacity due to latent inhibition. Structural equation modeling was used to determine the causal influences in an anatomical network of these regions and others thought to mediate latent inhibition, including the accumbens and entorhinal cortex. An uncoupling of ascending influences between auditory regions was observed in latent inhibition. There was also a reduced influence on the accumbens from the perirhinal cortex in both latent inhibition and extinction. The results suggest a specific network with a neural mechanism of latent inhibition that appears to involve sensory gating, as evidenced by modifications in metabolic capacity and effective connectivity between auditory regions and reduced perirhinal cortex influence on the accumbens. Keywords latent inhibition; metabolic mapping; structural equation modeling; cytochrome oxidase; sensory gating; perirhinal cortex; learning and memory In latent inhibition (LI), preexposure to a stimulus inhibits subsequent associations with that stimulus (Lubow and Moore, 1959). LI has been demonstrated in several behavioral paradigms in a variety of species, including humans, and is disrupted in schizophrenics (Lubow, 1989). Lesion and pharmacological studies have explored the neural mechanisms underlying LI and have identified several key brain regions. Conditioned drink suppression and eye blink conditioning studies demonstrated that lesions to the entorhinal cortex disrupt LI (Coutureau et al., 1999;Shohamy et al., 2000;Coutureau et al., 2002). Other studies using a conditioned Correspondence should be addressed to: Prof. F. Gonzalez-Lima, University of Texas at Austin, Department of Psychology, 1 University Station A8000, Austin, TX 78712-0187, USA. Phone (512) Fax (512) 471-4728, email: gonzalez-lima@mail.utexas.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will under...

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Metabolic Effects of Blocking Tone Conditioning on the Rat Auditory System

Cited by 27 publications

References 43 publications

Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning

Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning

Thalamic Reticular Nucleus Activation Reflects Attentional Gating during Classical Conditioning

Functional networks underlying latent inhibition learning in the mouse brain

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