P C Holland

Johns Hopkins University, Baltimore, MD, USA

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Publications (29)123.48 Total impact

  • Article: An analysis of licking microstructure in three strains of mice.
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    ABSTRACT: Mouse models of feeding provide a useful tool for elucidating the molecular pathways of energy regulation. The majority of studies in mice have been limited to intake analyses conducted over extended periods of time, which fail to distinguish between a variety of factors that influence nutrient intake. Using licking microstructure analyses we examined both the size and number of licking bursts for water, polycose, sucrose and lecithin in three strains of mice (C57BL/6J, 129Sv/ImJ and C57129F1 hybrids), using pause criteria (250-500, >500 and >1000 ms) that have previously been described in the rat. Burst size and number varied both as a function of tastant concentration and mouse strain; however, these differences were most evident with the >1000 ms pause criterion. Consistent with previous reports, during water consumption C57 mice showed longer mean interlick intervals, a larger number of bursts but reduced burst size relative to the two other strains. F1 mice showed larger burst sizes for polycose, while C57 mice displayed a greater number of bursts for both polycose and sucrose. Both 129 and F1 mice were insensitive to sucrose concentration, whereas C57 mice showed attenuated lecithin intake influenced by a reduction in the size of bursts for this tastant. These results suggest that these strains of mice display differences in the pattern of licking that are most evident with the use of larger pause criteria. These differences in licking behavior might reflect influences of genetic background on pre- and post-ingestive factors controlling intake, the reinforcing properties of each tastant, or native differences in licking style.
    Appetite 12/2009; 54(2):320-30. · 2.59 Impact Factor
  • Article: Temporally limited role of substantia nigra-central amygdala connections in surprise-induced enhancement of learning.
    H J Lee, J M Youn, M Gallagher, P C Holland
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    ABSTRACT: Prediction error plays an important role in modern associative learning theories. For example, the omission of an expected event (surprise) can enhance attention to cues that accompany those omissions, such that subsequent new learning about those cues is more rapid. Many studies from our laboratories have demonstrated that circuitry that includes the amygdala central nucleus (CeA), the cholinergic neurons in the substantia innominata/nucleus basalis region and their innervation of the posterior parietal cortex is critical for this surprise-induced enhancement of attention in learning. We recently showed that midbrain dopamine neurons, known to code prediction error, are also important for surprise-induced enhancement of learning through their interaction with CeA. The present study examined whether in rats the communication between the substantia nigra pars compacta (SNc) and CeA is critical only at the time of surprise, for example to detect prediction error information, or is also needed to maintain and later express that information as enhanced learning. All animals received unilateral CeA lesions and unilateral cannula implants targeting the SNc located contralateral to the lesioned CeA. As the SNc-CeA connections are mainly ipsilateral, inactivating SNc contralateral to the lesioned CeA provided transient blockage of SNc and CeA communication. The results show that SNc-CeA communication is critical for processing prediction error information at the time of surprise, but neither SNc nor SNc-CeA communication is necessary to express that information as enhanced learning later.
    European Journal of Neuroscience 07/2008; 27(11):3043-9. · 3.63 Impact Factor
  • Article: Inhibitory learning tests of conditioned stimulus associability in rats with lesions of the amygdala central nucleus.
    P C Holland, Y Chik, Q Zhang
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    ABSTRACT: Normal rats showed faster inhibitory learning about a light conditioned stimulus (CS) if it had previously been an inconsistent predictor of a tone CS than if it had been a consistent predictor of the tone. In contrast, the inhibitory learning of rats with ibotenic acid lesions of the amygdala central nucleus (CN) was unaffected by the prior predictive value of the light. These results support claims that the CN is critical to surprise-induced enhancement of attentional processing of CSs.
    Behavioral Neuroscience 11/2001; 115(5):1154-8. · 2.62 Impact Factor
  • Article: Rats with basolateral amygdala lesions show normal increases in conditioned stimulus processing but reduced conditioned potentiation of eating.
    P C Holland, T Hatfield, M Gallagher
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    ABSTRACT: Rats with neurotoxic lesions of basolateral amygdala (ABL) and control rats showed comparable enhancement of attentional processing of a visual stimulus when its predictive value was altered. In contrast, lesioned rats showed less potentiation of eating than did control rats when food was available during presentations of a conditioned stimulus that was previously paired with food. When considered together with previous data, these results indicate a double dissociation between effects of lesions of the ABL and of the amygdala central nucleus on phenomena related to attentional processing and the acquisition of motivational value.
    Behavioral Neuroscience 09/2001; 115(4):945-50. · 2.62 Impact Factor
  • Article: The influence of associability changes in negative patterning and other discriminations.
    P C Holland, J A Thornton, L Ciali
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    ABSTRACT: Normal rats showed faster learning of a serial negative patterning (NP) discrimination (X+, A+, X-->A-) than of a comparable feature negative (FN) discrimination (A+, X-->A-). This advantage was absent in rats with lesions of the amygdala central nucleus. Earlier data indicated that this brain lesion interferes with surprise-induced increases in attention specified by the Pearce-Hall model (J. M. Pearce & G. Hall, 1980). In the NP task, but not the FN task, omission of the reinforcer after X on X-->A- trials was surprising. A variation of the NP task (NPX), in which X was reinforced on both X+ and X-->A- trials, was learned more rapidly than the NP task. Lesioned rats were unimpaired in learning the NPX task. Evaluation of the lesion effects and the results of posttraining transfer tests suggested that the NP advantage involved attentional processes, whereas the NPX advantage was based on the acquisition of inhibitory control by aspects of excitation conditioned to X.
    Journal of Experimental Psychology Animal Behavior Processes 11/2000; 26(4):462-76. · 2.05 Impact Factor
  • Article: Lesions of the amygdala central nucleus alter performance on a selective attention task.
    P C Holland, J S Han, M Gallagher
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    ABSTRACT: Previous studies showed a role for the amygdala central nucleus (CN) in attentional processing during the acquisition of Pavlovian associations. Both the acquisition of conditioned orienting responses and the surprise-induced enhancement in the ability of conditioned stimuli to enter into new associations depend on the integrity of CN. In this experiment, the role of CN in the performance of a well-learned selective attention task was examined. Rats with ibotenic acid lesions of CN and control rats first learned a discrete-trial, multiple-choice reaction time task. On each trial, after a constant-duration ready signal, the rats were required to poke their noses into one of three ports, guided by the brief illumination of one of those ports. Rats with CN lesions were slower to acquire the task than control rats but showed equivalent asymptotic sustained performance. Subsequent attentional challenges, which included reducing the duration of the port illumination and varying the duration of the ready signal, had greater impact on the performance of lesioned than control rats. These data resemble those reported from similar tasks after damage to the basal forebrain (BF) system. Together with earlier findings, these data support a role for CN in modulating visuospatial attention in action as well as in the acquisition of associations, perhaps by way of its projections to BF cholinergic systems.
    Journal of Neuroscience 10/2000; 20(17):6701-6. · 7.11 Impact Factor
  • Article: Overshadowing and blocking as acquisition deficits: no recovery after extinction of overshadowing or blocking cues.
    P C Holland
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    ABSTRACT: The effects of extinction of the blocking or overshadowing stimulus on conditioned responding controlled by the blocked or overshadowed stimulus were examined in seven appetitive conditioning experiments with rats. The experiments differed in their designs, stimuli used, the amounts of conditioning and extinction training, and the levels of conditioned responding produced. In all cases, conditioned responding to the blocked or overshadowed cue was either unaffected or reduced by extinction of the blocking or overshadowing cue. These data are consistent with accounts of overshadowing and blocking that attribute those phenomena to acquisition deficits, rather than to retrieval failures.
    The Quarterly Journal of Experimental Psychology 12/1999; 52(4):307-33. · 4.67 Impact Factor
  • Article: Blocking can occur without losses in attention in rats with selective removal of hippocampal cholinergic input.
    M G Baxter, M Gallagher, P C Holland
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    ABSTRACT: Prior studies showed that 192 IgG-saporin lesions of cholinergic input to the hippocampus disrupted reductions in processing of uninformative stimuli. In 2 experiments in this study, the performance of rats with these lesions was examined in blocking procedures. In both lesioned and normal rats, previous pairing of one conditioned stimulus (CS) with food blocked conditioning of a 2nd CS when a compound of both CSs was paired with food. However, in subsequent savings tests, lesioned rats showed faster learning than did normal rats when the blocked CS was established as a signal for either reinforcement or nonreinforcement. Thus, the reduced attention to the blocked CS found in normal but not lesioned rats was not essential for the occurrence of blocking. Although rats with selective removal of hippocampal cholinergic input may be unable to reduce attention to redundant stimuli, other mechanisms of stimulus selection remain available to them.
    Behavioral Neuroscience 11/1999; 113(5):881-90. · 2.62 Impact Factor
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    Article: Impairments in conditioned stimulus processing and conditioned responding after combined selective removal of hippocampal and neocortical cholinergic input.
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    ABSTRACT: Previous studies indicated that changes in attentional processing of conditioned stimuli (CSs) are regulated by the basal forebrain (BF) cholinergic system. In those studies, destruction of BF innervation of the neocortex interfered with enhancements in CS processing, and destruction of BF innervation of the hippocampus prevented reductions in CS processing. In the current experiments, the performance of rats with 192 IgG-saporin lesions of both hippocampal and neocortical cholinergic input was examined. These combined lesions disrupted both enhancements and reductions in CS processing. Lesioned rats also showed more general impairments in conditioned responding. These results indicate that, although the neural systems for increasing and decreasing attentional processing may be largely independent, combined loss of hippocampal and neocortical cholinergic input may produce behavioral impairments that are not apparent after either lesion alone.
    Behavioral Neuroscience 07/1999; 113(3):486-95. · 2.62 Impact Factor
  • Article: Hippocampus and context in classical conditioning.
    P C Holland, M E Bouton
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    ABSTRACT: Recent evidence suggests that contextual learning encompasses a variety of changes in learning and performance processes. Only some of these changes depend on the hippocampus. Specialized functions proposed for the hippocampus in contextual learning include the construction and consolidation of contextual memory representations, incidental contextual learning, and inhibitory contextual learning.
    Current Opinion in Neurobiology 05/1999; 9(2):195-202. · 7.44 Impact Factor
  • Article: Disconnection of the amygdala central nucleus and substantia innominata/nucleus basalis disrupts increments in conditioned stimulus processing in rats.
    J S Han, P C Holland, M Gallagher
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    ABSTRACT: Rats with a neurotoxic lesion of the amygdala central nucleus (CN) in one hemisphere and a 192 immunoglobulin G (192IgG)-saporin lesion of cholinergic neurons in the contralateral substantia innominata/nucleus basalis (SI/nBM) failed to show the enhanced attentional processing of a conditioned stimulus (CS) observed in sham-operated rats when that CS's predictive value was altered. Performance of these asymmetrically lesioned rats was poorer than that of rats with a unilateral lesion of either structure or with a symmetrical lesion of both structures in the same hemisphere. These results implicate connections between the CN and SI/nBM in the incremental attentional processing of CSs, extending previous research that has shown similar effects of bilateral lesions of either the CN or the SI/nBM.
    Behavioral Neuroscience 03/1999; 113(1):143-51. · 2.62 Impact Factor
  • Article: Hippocampal lesions interfere with Pavlovian negative occasion setting.
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    ABSTRACT: Rats were trained with either a serial feature positive (L-->T1+ T-) or a serial feature negative (L-->T1-, T1+) discrimination, intermixed with training on another, nonconditional discrimination (T2+, N-), using a Pavlovian appetitive conditioning preparation with multiple response measures. Among rats trained with the serial feature positive discrimination, neurotoxic lesions of the hippocampus produced a transient impairment in the acquisition of that discrimination, but did not affect acquisition of the nonconditional discrimination. In contrast, among rats that received serial feature negative discrimination training, hippocampal lesions produced enduring deficits in the acquisition of both discriminations. The results of transfer tests indicated that both lesioned and control rats used a conditional learning strategy (occasion setting) to solve the feature positive and feature negative discriminations. Furthermore, lesioned rats, especially those that received training with the feature negative discrimination, displayed increasingly higher levels of general activity as training progressed. The results suggest that hippocampal lesions particularly interfere with inhibitory learning (negative occasion setting) about both explicit and contextual cues.
    Hippocampus 01/1999; 9(2):143-57. · 5.18 Impact Factor
  • Article: Removal of cholinergic input to rat posterior parietal cortex disrupts incremental processing of conditioned stimuli.
    D J Bucci, P C Holland, M Gallagher
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    ABSTRACT: Recent research suggests that the basal forebrain cholinergic neurons innervating the cortex play a role in attentional functions in both primates and rodents. Among the cortical targets of these projections in primates is the posterior parietal cortex (PPC), a region shown to be critically involved in the regulation of attention. Recent anatomical studies have defined a cortical region in the rat that may be homologous to the PPC of primates. In the present study, cholinergic innervation of the PPC was depleted by intracortical infusion of the immunotoxin 192 IgG-saporin. Control and lesioned rats were then tested in two associative learning paradigms designed to increase attentional processing of conditioned stimuli (CSs). In one experiment, attention was manipulated by shifting a predictive relation between a light CS and another CS to a less predictive relation. Unlike control rats, lesioned rats failed to increase attention when the predictive relation was modified. In a second experiment, attentional processing of a tone CS was increased when its introduction during training coincided with a change in the value of the unconditioned stimulus, a phenomenon referred to as unblocking. Unlike control rats, lesioned rats failed to exhibit unblocking. In both paradigms, lesioned rats conditioned normally when the training procedures did not encourage increased attentional processing. These findings, across different behavioral paradigms and stimulus modalities, provide converging evidence that intact cholinergic innervation of the PPC is important for changes in attention that can increase the processing of certain cues.
    Journal of Neuroscience 11/1998; 18(19):8038-46. · 7.11 Impact Factor
  • Article: Occasion setting: a neural network approach.
    N A Schmajuk, J A Lamoureux, P C Holland
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    ABSTRACT: Classical conditioning data show that a conditioned stimulus (CS) can act either as a simple CS--eliciting conditioned responses (CRs) by signaling the occurrence of an unconditioned stimulus (US)--or as an occasion setter--controlling the responses generated by another CS. In this article, the authors apply a simple extension of a network model of conditioning, originally presented by N. A. Schmajuk and J. J. DiCarlo (S-D; 1992), to the description of these 2 different CS functions. In the model, CS inputs are connected to the CR output both directly and indirectly through a hidden unit layer that codes configural stimuli. In this framework, a CS acts as (a) a simple stimulus through its direct connections with the output units and as (b) an occasion setter through its indirect configural connections via the hidden units. Computer simulations demonstrate that the network accounts for a large part of the data on occasion setting.
    Psychological Review 02/1998; 105(1):3-32. · 7.76 Impact Factor
  • Article: Neurotoxic hippocampal lesions fail to impair reinstatement of an appetitively conditioned response.
    G D Fox, P C Holland
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    ABSTRACT: Rats with ibotenate lesions of the hippocampus (HPC) and nonlesioned rats were trained with a Pavlovian appetitive conditioning procedure in which a visual conditioned stimulus (CS) was first paired with a food unconditioned stimulus (US) and then repeatedly presented in the absence of the food US. After extinction of the conditioned response (CR), half of the rats received presentations of the food US and half did not. On a final test of responding to the visual CS, rats that received the postextinction US presentations showed higher levels of conditioned responding than the rats that did not. This reinstatement of CRs was not affected by the HPC lesions, which nevertheless impaired performance on a water maze task known to be sensitive to HPC damage. These data are in contrast to those of A. Wilson, D. C. Brooks, and M. E. Bouton (1995), who found that lesions of the fornix abolished reinstatement of aversively conditioned behavior.
    Behavioral Neuroscience 02/1998; 112(1):255-60. · 2.62 Impact Factor
  • Article: Disruption of decrements in conditioned stimulus processing by selective removal of hippocampal cholinergic input.
    M G Baxter, P C Holland, M Gallagher
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    ABSTRACT: The attention directed to environmental stimuli can be modified by experience. For example, preexposure of a conditioned stimulus (CS) in the absence of reinforcement can retard subsequent conditioning of that stimulus when it is paired directly with an unconditioned stimulus, a phenomenon referred to as latent inhibition. Similarly, consistent pairings of a CS with another event can slow the acquisition of new information about that CS. Such phenomena suggest that reductions in the processing of CSs occur when they are made behaviorally irrelevant or consistent predictors of other events. On the basis of the observation that hippocampal lesions prevented such reductions in CS processing, we hypothesized that damage to basal forebrain cholinergic neurons that project to the hippocampus, using microinjections of the selective immunotoxin 192 IgG-saporin into the medial septum/vertical limb of the diagonal band (MS/VDB), also would disrupt normal reductions in CS processing. Lesions of hippocampal cholinergic input disrupted decreases in CS processing, manifested in both an absence of latent inhibition and a lack of reduced processing of a CS that had been a consistent predictor of another CS. These results indicate that cholinergic neurons in the MS/VDB play a role in the regulation of CS processing. Furthermore, these findings (in conjunction with previous findings) implicate both rostral (hippocampal-projecting) and caudal (cortical-projecting) regions of the basal forebrain cholinergic system in the modulation of attention.
    Journal of Neuroscience 08/1997; 17(13):5230-6. · 7.11 Impact Factor
  • Article: Temporal specificity in serial feature-positive discrimination learning.
    P C Holland, P A Hamlin, J P Parsons
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    ABSTRACT: Two experiments examined the temporal specificity of learning in operant serial feature-positive discriminations (feature-->target+/target-). Test performance was better when the target cues were presented at their customary times after the features than when they were presented at earlier or later times. When features trained with one feature-target interval were combined with targets trained with another interval, performance was best when the test interval was the same as the interval associated with the feature, suggesting that the temporal information was coded with the feature cue. Finally, the temporal specificity of the responding controlled by occasion setters was unaffected by feature extinction. Implications for the nature of learning in occasion setting are discussed.
    Journal of Experimental Psychology Animal Behavior Processes 01/1997; 23(1):95-109. · 2.05 Impact Factor
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    Article: Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing.
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    ABSTRACT: Magnocellular neurons in the basal forebrain provide the major cholinergic innervation of cortex. Recent research suggests that this cholinergic system plays an important role in the regulation of attentional processes. The present study examined the ability of rats with selective immunotoxic lesions of these neurons (made with 192 IgG-saporin) to modulate attention within an associative learning framework. Each rat was exposed to conditioned stimuli (CS) that were either consistent or inconsistent predictors of subsequent cues. Intact control rats showed increased CS associability when that cue was an inconsistent predictor of a subsequent cue, whereas lesioned rats were impaired in increasing attention to the CS when its established relation to another cue was modified. In a separate experiment designed to test latent inhibition, it was shown that removal of the corticopetal cholinergic neurons spared a decrement in associability that occurs when rats are extensively preexposed to a CS prior to conditioning. These data indicate that the cholinergic innervation of cortex is critical for incrementing, but not for decrementing attentional processing. The specific behavioral tests used to assess the role of the basal forebrain cholinergic system in the present study were previously used to identify a role for the amygdala central nucleus in attention (Holland and Gallagher, 1993b). Those studies, together with the results in this report, indicate that regulation of attentional processes during associative learning may be mediated by projections from the amygdala to the basal forebrain cholinergic system.
    Journal of Neuroscience 12/1995; 15(11):7315-22. · 7.11 Impact Factor
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    Article: The amygdala complex: multiple roles in associative learning and attention.
    M Gallagher, P C Holland
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    ABSTRACT: Although certain neurophysiological functions of the amygdala complex in learning seem well established, the purpose of this review is to propose that an additional conceptualization of amygdala function is now needed. The research we review provides evidence that a subsystem within the amygdala provides a coordinated regulation of attentional processes. An important aspect of this additional neuropsychology of the amygdala is that it may aid in understanding the importance of connections between the amygdala and other neural systems in information processing.
    Proceedings of the National Academy of Sciences 01/1995; 91(25):11771-6. · 9.68 Impact Factor
  • Article: Cognitive aspects of classical conditioning.
    P C Holland
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    ABSTRACT: Cognitive processes have been increasingly implicated in Pavlovian conditioning. Research in the past year has focused on questions of stimulus selection and the internal representation of events and the relations between them. Recent data support negative feedback models of selection that assume conditioning-dependent changes in processing of conditioned and unconditioned stimulus events, and suggest potential neural mechanisms that may underlie these processes. New models of conditioning propose a more detailed representation of individual conditioning episodes than traditionally assumed. The results of investigations into conditional discrimination learning imply a hierarchical organization of event representations, and illustrate the importance of conditioned modulatory processes as distinct from response elicitation.
    Current Opinion in Neurobiology 05/1993; 3(2):230-6. · 7.44 Impact Factor

Institutions

  • 1999–2009
    • Johns Hopkins University
      • Department of Psychological & Brain Sciences
      Baltimore, MD, USA
    • Harvard University
      • Department of Psychology
      Cambridge, MA, USA
  • 1988–2001
    • Duke University
      Durham, NC, USA
  • 1990–1999
    • University of North Carolina at Chapel Hill
      • Department of Psychology
      Chapel Hill, NC, USA