Background Firing Rates of Orbitofrontal Neurons Reflect Specific Characteristics of Operant Sessions and Modulate Phasic Responses to Reward-Associated Cues and Behavior

ArticleinThe Journal of Neuroscience : The Official Journal of the Society for Neuroscience 28(4):1009-18 · February 2008with3 Reads
Impact Factor: 6.34 · DOI: 10.1523/JNEUROSCI.4344-07.2008 · Source: PubMed
Abstract

The orbitofrontal cortex plays an important role in the ability of animals to adjust their behavior in response to behavioral outcomes. Multiple studies have demonstrated that responses of orbitofrontal neurons during operant sessions reflect the outcome of particular behaviors. These studies have focused on rapid neural responses to short-duration events such as instrumental behavior and reward-associated discrete cues. We hypothesize that longer-lasting changes in firing are also important for information processing in the orbitofrontal cortex. In the present study, we recorded the activity of 115 single orbitofrontal neurons during a multiphase operant task in which the relationship between a lever-press response and a sucrose reward was varied between the different phases. Approximately one-half of the orbitofrontal neurons exhibited a change in background firing during the operant phases. These changes were observable across multiple behavioral and stimulus events and thus reflected a general shift in background firing. The majority of changes were selective for one or the other of the operant phases. Selective changes contributed to unique patterns of phasic firing time locked to cues and operant behavior in the two operant phases. These findings are consistent with the interpretation that changes in background firing of orbitofrontal neurons reflect operant session characteristics associated with behavioral outcome, and indicate further that changes in background firing contribute to the outcome selectivity of phasic firing patterns. More generally, we propose that the background firing rates of orbitofrontal neurons reflect contextual information, and facilitate context-appropriate event-related information processing and behavioral responses.

    • "...Arana et al., 2003; Caplan et al., 2007; Elliott et al., 2000; Frey and Petrides, 2002; Kravitz and Peoples, 2008; LoPresti et al., 2008; Murray and Izquierdo, 2007; O'Doherty et al., 2003; Schon et al., 2008; You..."
      Among prefrontal structures, the OFC is a unique site of convergence for sensory and reward information, receiving input from every sensory modality (Barbas, 2000) and sharing strong connections with the amygdala and the nucleus accumbens (Cavada et al., 2000; Roberts et al., 2007; Thierry et al., 2000). This distinct pattern of anatomical connections supports the functional role of the OFC in processing contextual information, flexible behavior, guiding response selection, and the resolution of interference (Arana et al., 2003; Caplan et al., 2007; Elliott et al., 2000; Frey and Petrides, 2002; Kravitz and Peoples, 2008; LoPresti et al., 2008; Murray and Izquierdo, 2007; O'Doherty et al., 2003; Schon et al., 2008; Young and Shapiro, 2011).
    [Show abstract] [Hide abstract] ABSTRACT: Research in animals and humans has demonstrated that the hippocampus is critical for retrieving distinct representations of overlapping sequences of information. There is recent evidence that the caudate nucleus and orbitofrontal cortex are also involved in disambiguation of overlapping spatial representations. The hippocampus and caudate are functionally distinct regions, but both have anatomical links with the orbitofrontal cortex. The present study used an fMRI-based functional connectivity analysis in humans to examine the functional relationship between the hippocampus, caudate, and orbitofrontal cortex when participants use contextual information to navigate well-learned spatial routes which share common elements. Participants were trained outside the scanner to navigate virtual mazes from a first-person perspective. Overlapping condition mazes began and ended at distinct locations, but converged in the middle to share some hallways with another maze. Non-overlapping condition mazes did not share any hallways with any other maze. Successful navigation through the overlapping hallways required contextual information identifying the current navigational route to guide the appropriate response for a given trial. Results revealed greater functional connectivity between the hippocampus, caudate, and orbitofrontal cortex for overlapping mazes compared to non-overlapping mazes. The current findings suggest that the hippocampus and caudate interact with prefrontal structures cooperatively for successful contextually dependent navigation.
    Full-text · Article · Jan 2012 · NeuroImage
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    • "...al., 2007). An emerging body of literature in both animals (Murray and Izquierdo, 2007; Kravitz and Peoples, 2008) and humans (Elliott et al., 2000; Frey and Petrides, 2002; Arana et al., 2003; O'Doherty et al., 2..."
      The orbitofrontal cortex receives input from every sensory modality (Barbas, 2000) and is anatomically connected with the hippocampus directly (Barbas and Blatt, 1995; Cavada et al., 2000; Catenoix et al., 2005; Roberts et al., 2007), and through connections with the adjacent entorhinal and perirhinal cortices (Cavada et al., 2000; Kondo et al., 2005; Roberts et al., 2007). An emerging body of literature in both animals (Murray and Izquierdo, 2007; Kravitz and Peoples, 2008) and humans (Elliott et al., 2000; Frey and Petrides, 2002; Arana et al., 2003; O'Doherty et al., 2003; Caplan et al., 2007; LoPresti et al., 2008; Schon et al., 2008) suggests that the orbitofrontal cortex processes contextual information and is important for promoting flexible behavior, guiding response selection, and the resolution of interference. One patient with a lesion which included the orbitofrontal cortex was unable to suppress habitual responses at intersections in favor of the correct direction, despite being able to recall the correct destination (Ciaramelli, 2008).
    [Show abstract] [Hide abstract] ABSTRACT: Groundbreaking research in animals has demonstrated that the hippocampus contains neurons that distinguish between overlapping navigational trajectories. These hippocampal neurons respond selectively to the context of specific episodes despite interference from overlapping memory representations. The present study used functional magnetic resonance imaging in humans to examine the role of the hippocampus and related structures when participants need to retrieve contextual information to navigate well learned spatial sequences that share common elements. Participants were trained outside the scanner to navigate through 12 virtual mazes from a ground-level first-person perspective. Six of the 12 mazes shared overlapping components. Overlapping mazes began and ended at distinct locations, but converged in the middle to share some hallways with another maze. Non-overlapping mazes did not share any hallways with any other maze. Successful navigation through the overlapping hallways required the retrieval of contextual information relevant to the current navigational episode. Results revealed greater activation during the successful navigation of the overlapping mazes compared with the non-overlapping mazes in regions typically associated with spatial and episodic memory, including the hippocampus, parahippocampal cortex, and orbitofrontal cortex. When combined with previous research, the current findings suggest that an anatomically integrated system including the hippocampus, parahippocampal cortex, and orbitofrontal cortex is critical for the contextually dependent retrieval of well learned overlapping navigational routes.
    Full-text · Article · May 2010 · The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
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    • "...arry information which the animal (or human) has already learned about the stimulation (Kravitz and Peoples 2008) and therefore may reflect active (although not necessarily specific) anticipation of stimuli. Howe..."
      Growing evidence shows that ongoing activity significantly affects how animals (Arieli et al. 1996) and humans (Romei et al. 2007) respond to sensory stimulation. Ongoing activity may carry information which the animal (or human) has already learned about the stimulation (Kravitz and Peoples 2008) and therefore may reflect active (although not necessarily specific) anticipation of stimuli. However, in psychophysical experiments, anticipation is typically minimized such that ongoing activity could be treated as mere variability.
    [Show abstract] [Hide abstract] ABSTRACT: We investigated the relationship between visual experience and temporal intervals of synchronized brain activity. Using high-density scalp electroencephalography, we examined how synchronized activity depends on visual stimulus information and on individual observer sensitivity. In a perceptual grouping task, we varied the ambiguity of visual stimuli and estimated observer sensitivity to this variation. We found that durations of synchronized activity in the beta frequency band were associated with both stimulus ambiguity and sensitivity: the lower the stimulus ambiguity and the higher individual observer sensitivity the longer were the episodes of synchronized activity. Durations of synchronized activity intervals followed an extreme value distribution, indicating that they were limited by the slowest mechanism among the multiple neural mechanisms engaged in the perceptual task. Because the degree of stimulus ambiguity is (inversely) related to the amount of stimulus information, the durations of synchronous episodes reflect the amount of stimulus information processed in the task. We therefore interpreted our results as evidence that the alternating episodes of desynchronized and synchronized electrical brain activity reflect, respectively, the processing of information within local regions and the transfer of information across regions.
    Full-text · Article · Aug 2009 · Cerebral Cortex
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  • [Show abstract] [Hide abstract] ABSTRACT: Based on neuro-imaging studies in cocaine-addicted humans, it is hypothesized that increases in neural activity within several regions of the prefrontal cortex contribute to cue-induced cocaine seeking and cocaine-induced compulsive drug self-administration. However, electrophysiological tests of these hypotheses are lacking. In the present study, animals were trained to self-administer cocaine (0.75 mg/kg) for 14 days. On the 14th day, we conducted electrophysiological recordings of lateral orbitofrontal (LO) and ventral anterior insula (AIV) neurons. A subset of the combined population of recorded neurons showed a change in firing rate in association with one or more of the following discrete events: (1) presentation of a discriminative stimulus that signaled the onset of the self-administration session, (2) occurrence of the first cocaine-directed operant response, (3) occurrence of a cocaine-reinforced press, and (4) presentation of cues normally paired with delivery of the cocaine reinforcer. The majority of the stimulus- and response-related changes in firing involved a brief increase in firing during the stimulus and response event, respectively. In addition to these event-specific responses, approximately half of the recorded neurons exhibited a sustained change in average firing (i.e., discharges per 30-s bin) during the cocaine self-administration session, relative to average firing during a presession, drug-free period (referred to as session changes). The prevalence of session-increases and decreases were not significantly different. These and other findings are discussed in relation to hypotheses about cue-evoked and cocaine-maintained cocaine-directed behavior.
    Full-text · Article · Jan 2010 · Synapse
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  • [Show abstract] [Hide abstract] ABSTRACT: This paper seeks to elucidate the design and implementation of an instrumentation amplifier, filters, LabVIEW-based spike detection, and automatic spike counting to detect pleasure sensation in the rat using invasive BCI. This method involved sites related to pleasure, and after acquiring signals from the ventral pallidum, facial motor cortex, and orbitofrontal cortex, these signals were analyzed to assess the pleasure sensation in the rat. The results illustrated a decreased spike rate in the motor and orbitofrontal cortices and an increased spike rate in the ventral pallidum during pleasure. The pleasure detection experiment was conducted four times to obtain the mean values of spike rates. The motor cortex had 9spikes/s, the orbitofrontal cortex had 18spikes/s and the ventral pallidum had 34spikes/s. The correlation coefficient is above 78%, effectiveness of the experiment.
    No preview · Article · Jan 2011 · Measurement
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  • [Show abstract] [Hide abstract] ABSTRACT: Functional magnetic resonance imaging (fMRI) and single unit physiology are two of the most widely-used methods in cognitive neuroscience and neuroeconomics. Despite the fact that practitioners of both methods share a common goal - understanding the mechanisms underlying behaviour and cognition - their efforts are rarely directly linked. This chapter considers some of the reasons for apparent discrepancies between findings of fMRI and electrophysiological studies. It examines these problems through the lens of two case studies - decision making under uncertainty and fictive learning - derived from personal research. Despite this narrow focus, these arguments can extend to other areas of study. It is shown that major differences in the neural events measured by the two methods, the behavioural techniques employed with animal and human subjects, and the intellectual history and unique culture of each discipline, contribute to difficulties in providing a wholly synthetic account of the mechanisms underlying cognition and decision making. These observations endorse more collaborative efforts conducting parallel research using analogous, if not identical, behavioural techniques using both brain imaging and single unit physiology. © The International Association for the study of Attention and Performance, 2011. All rights reserved.
    No preview · Article · Mar 2011
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