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

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 rewardassociated 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.

Orbitofrontal and insular cortex: Neural responses to cocaine-associated cues and cocaine self-administration

“…The findings of the present study extend other electrophysiological rat studies of orbitofrontal cortex, which demonstrate that orbitofrontal neurons show responses associated with operant behavior (Feierstein et al, 2006;Furuyashiki et al, 2008;Kravitz and Peoples, 2008;Tremblay and Schultz, 2000b). Such responses have not been observed in primate recording studies of the orbitofrontal cortex (Critchley and Rolls, 1996;Roesch and Olson, 2004;Schoenbaum et al, 1999;Schultz, 1999, 2000a).…”

“…A stable change in average firing during the same period potentially corresponds to an acute pharmacological effect of cocaine. We thus tested for stable changes in firing during the session relative to the presession, drug-free period (referred to as a session change) (Kravitz et al, 2006;Kravitz and Peoples, 2008;Peoples et al, 1998b). To test for a significant session-change, firing rate (i.e., Hertz per 30-s bin) was calculated for the 60-min presession baseline period and for the last 120 min of the self-administration session (i.e., the maintenance phase of the self-administration session).…”

Cooperative interactions between hippocampal and striatal systems support flexible navigation

“…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). …”

“…The orbitofrontal cortex is a critical structure for goal-directed behavior, and supports flexible response selection and suppression in animals (Murray and Izquierdo, 2007) and humans (Arana et al, 2003; Elliott et al, 2000; O'Doherty et al, 2003). Orbitofrontal neurons have been shown to encode both rewarding and aversive stimuli (Morrison and Salzman, 2009) and their firing patterns adapt to reflect changes in context (Kravitz and Peoples, 2008; Simmons and Richmond, 2008). The rodent orbitofrontal cortex codes for goal-directed paths and exhibits oscillatory coherence with the hippocampus during goal-directed navigation (Young and Shapiro, 2011).…”

Which Way Was I Going? Contextual Retrieval Supports the Disambiguation of Well Learned Overlapping Navigational Routes

“…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).…”