Associative effects of Pavlovian differential inhibition of behaviour

Jones, Dirk; González-Lima, Francisco

doi:10.1046/j.0953-816x.2001.01810.x

Cited by 17 publications

(13 citation statements)

References 51 publications

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“…Cued conditioned group showed a relative CO activity decrease in the hippocampal regions examined, suggesting that changes in neural metabolism in this brain area associated with aversive auditory cued conditioning depend on the learned value of the tone CS. Our data is supported by other studies which also demonstrated a decrease in hippocampal CO activity following Pavlovian fear conditioning (Conejo et al, 2005), and conditioned response inhibition (Jones and Gonzalez-Lima, 2001). Additionally, local cerebral perfusion is decreased in response to a fear conditioned tone CS (Holschneider et al, 2006), and neurotoxic lesions of the dorsal hippocampus have been found to impair cued Pavlovian conditioning in rats (Maren et al, 1997), further indicating that dorsal hippocampus plays an important role in the Pavlovian fear conditioning in rats.…”

Section: Discussionsupporting

confidence: 92%

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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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Section: Discussionsupporting

confidence: 92%

“…Possible optical artifacts from the camera were corrected through background subtraction. A calibration curve was created with the standards using a single regression equation (Jones and Gonzalez-Lima, 2001) in order to account for between-batch staining differences. These standards were linear in the 10 to 80 micron range of thickness used.…”

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confidence: 99%

Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning

Bruchey

González-Lima

2008

Neuroscience

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“…The present study continues to emphasize the importance of hippocampal and parahippocampal regions in converging auditory (CS) and somatosensory (US) information. Another study on differential inhibition (Jones and Gonzalez-Lima, 2001a) showed decreased activity in the ventral cochlear nucleus in the differential inhibition group, which reflects changes in the learned signal value of the tone. Similarly in LI, the learned signal value of the tone decreases as the tone becomes an irrelevant stimulus that does not provide any new information about the environment.…”

Section: Discussionmentioning

confidence: 94%

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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“…Zonal analyses of cytochrome oxidase activity of lesions in the unilateral lesion model (group x lesion zone) were done with factorial ANOVA with staining batch as a covariate. Differences in interregional functional interactions were calculated according to the method of Jones and Gonzalez Lima (2001). Pearson correlations between cytochrome oxidase activity in the regions of interest were obtained.…”

Section: Methodsmentioning

confidence: 99%

Striatal neuroprotection with methylene blue

et al. 2009

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Recent literature indicates that low-dose methylene blue (MB), an autoxidizable dye with powerful antioxidant and metabolic enhancing properties, might prevent neurotoxin-induced neural damage and associated functional deficits. This study evaluated whether local MB may counteract the anatomical and functional effects of the intrastriatal infusion of the neurotoxin rotenone in the rat. To this end, stereological analyses of striatal lesion volumes were performed and changes in oxidative energy metabolism in the striatum and related motor regions were mapped using cytochrome oxidase histochemistry. The influence of MB on striatal levels of oxidative stress induced by rotenone was determined, and behavioral tests were used to investigate the effect of unilateral MB coadministration on motor asymmetry. Rotenone induced large anatomical lesions resembling "metabolic strokes", whose size was greatly reduced in MB-treated rats. Moreover, MB prevented the decrease in cytochrome oxidase activity and the perilesional increase in oxidative stress associated with rotenone infusion in the striatum. MB also prevented the indirect effects of the rotenone-induced lesion on cytochrome oxidase activity in related motor regions, such as the striatal regions rostral and caudal to the lesion, the substantia nigra compacta and reticulata, and the pedunculopontine nucleus. At a network level, MB maintained a global strengthening of functional connectivity in basal ganglia-thalamocortical motor circuits, as opposed to the functional decoupling observed in rotenone-alone subjects. Finally, MB partially prevented the behavioral sensorimotor asymmetries elicited by rotenone. These results are consistent with protective effects of MB against neurotoxic damage in the brain parenchyma. This study provides the first demonstration of the anatomical, metabolic and behavioral neuroprotective effects of MB in the striatum in vivo, and supports the notion that MB could be a valuable intervention against neural damage associated with oxidative stress and energy hypometabolism. Corresponding author: Prof. Dr. F. Gonzalez-Lima, University of Texas at Austin, 1 University Station A8000, Austin, TX 78712, 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 undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access Author ManuscriptNeuroscience. Author manuscript; available in PMC 2010 October 20. Published in final edited form as:Neuroscience. (Bruchey and Gonzalez-Lima, 2008). MB has been widely used as a supravital stain of nervous tissue (O'Leary et al., 1968), as well as an artificial electron donor (Lindahl and Oberg, 1961, Lehninger, 1964, ...

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Associative effects of Pavlovian differential inhibition of behaviour

Cited by 17 publications

References 51 publications

Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning

Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning

Functional networks underlying latent inhibition learning in the mouse brain

Striatal neuroprotection with methylene blue

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