Ventromedial and Orbital Prefrontal Neurons Differentially Encode Internally and Externally Driven Motivational Values in Monkeys

Abstract

The value of events that predict future rewards, thereby driving behavior, is sensitive to information arising from external (environmental) and internal factors. The ventral prefrontal cortex, an anatomically heterogeneous area, has information related to this value. We designed experiments to compare the contribution of two distinct subregions, orbital and ventromedial, of the ventral prefrontal cortex to the encoding of internal and external factors controlling the perceived motivational value. We recorded the activity of single neurons in both regions in monkeys while manipulating internal and external factors that should affect the perceived value of task events. Neurons in both regions encoded the value of task events, with orbitofrontal neurons being more sensitive to external factors such as visual cues and ventromedial neurons being more sensitive to internal factors such as satiety. Thus, the orbitofrontal cortex emphasizes signals for evaluating environment-centered, externally driven motivational processes, whereas ventromedial prefrontal cortex emphasizes signals more suited for subject-centered, internally driven motivational processes.

Connectivity reveals relationship of brain areas for reward-guided learning and decision making in human and monkey frontal cortex

“…Combining insights from human fMRI and animal studies is, however, not straightforward because there is uncertainty about basic issues, such as anatomical and functional correspondences between species (1). For example, although there are many reports of decision value-related activity in the human ventromedial prefrontal cortex (vmPFC) (2,3), it is unclear whether they can be related to reports of reward-related activity either on the ventromedial surface of the frontal lobe (4,5), in the adjacent medial orbitofrontal sulcus (6), or indeed to any macaque brain area. It is claimed that some areas implicated in rewardguided decision making and learning, such as parts of anterior cingulate cortex (ACC), are not found in macaques (7), but such theories have never been formally tested.…”

Towards a neuroimaging biomarker of depression vulnerability

“…Relative to the more lateral orbitofrontal aspects of the ventral forebrain, the VMPFC is particularly involved in self-referential rather than conceptual or objective estimation of emotional significance [76].…”

Automated MRI Parcellation of the Frontal Lobe

“…While gyral-sulcal landmarks define cytoarchitectonically-and functionally-relevant discrete regions in many cortical areas (e.g., angular gyrus/area 39 of Brodmann/posterior inferior parietal lobule) (Bouret and Richmond 2010;Geyer, et al 2000;Tekin and Cummings 2002; Zilles 1990;Zilles, et al 1997), the major frontal gyri traverse multiple Ranta et al Page 2 Hum Brain Mapp. Author manuscript; available in PMC 2015 May 01.…”

“…Due to this wide range of complex brain functions, abnormalities in frontal lobe structure and function have been hypothesized to contribute to many neuropsychiatric disorders, including obsessive-compulsive disorder (OCD) (Tekin and Cummings 2002), depression and bipolar disorder (Tekin and Cummings 2002), schizophrenia (Shad, et al 2006;Suzuki, et al 2005;Yamasue, et al 2004), Down syndrome (Pinter, et al 2001;Porter, et al 2007), Rett syndrome (Carter, et al 2008), fragile X syndrome (Gothelf, et al 2008;Kates, et al 2002a), idiopathic autism (Acosta and Pearl 2004;Courchesne, et al 2007), Tourette syndrome (Fredericksen, et al 2002;Marsh, et al 2007) and Attention-Deficit/Hyperactivity disorder (ADHD) (Kelly, et al 2007;Nigg and Casey 2005;Shaw, et al 2007;Shaw, et al 2006;Sowell, et al 2003). In view of the size and functional heterogeneity of the frontal lobe (Fuster 1997), it is likely that abnormalities in distinct functional regions are preferentially associated with a particular disorder or with a specific aspect of that disorder.While gyral-sulcal landmarks define cytoarchitectonically-and functionally-relevant discrete regions in many cortical areas (e.g., angular gyrus/area 39 of Brodmann/posterior inferior parietal lobule) (Bouret and Richmond 2010;Geyer, et al 2000;Tekin and Cummings 2002; Zilles 1990;Zilles, et al 1997), the major frontal gyri traverse multiple Ranta et al Page 2 Hum Brain Mapp. Author manuscript; available in PMC 2015 May 01.…”

“…The theoretical foundations for the divisions used in our protocol include the sometimes divergent relationships between gyral/sulcal landmarks and cytoarchitectonical and functional organization of the cortex (Fischl, et al 2008;Geyer, et al 2000;Ongur, et al 2003; Zilles 1990;Zilles, et al 1997) and the increasing body of information on the functional relevance of discrete frontal sub-regions for neuropsychiatric disorders. The premotor and prefrontal modules are divided into several anatomo-physiologic sub-regions based on the foundations of traditional and more recent anatomical and functional literature (Bouret and Richmond 2010;Costafreda, et al 2006;Graziano and Aflalo 2007;Howard, et al 2003;Lacerda, et al 2003;McGlinchey-Berroth, et al 1995;Ongur, et al 2003;Rushworth, et al 2007;Rypma 2006;Tekin and Cummings 2002;Tzourio-Mazoyer, et al 2002).In two prior studies (Kates, et al 2002b;Ranta, et al 2009) we presented a manual frontal lobe parcellation protocol that relies on sulcal-gyral landmarks to delineate functionally distinct frontal sub-regions: i.e., primary motor cortex, anterior cingulate, deep white matter, premotor cortex regions (supplementary motor complex (SMC), frontal eye field (FEF) and lateral premotor cortex (LPM)) and prefrontal cortex (PFC) regions (medial PFC, dorsolateral PFC (DLPFC), inferior PFC, lateral orbitofrontal cortex (OFC) and medial OFC) (see Figures 1 and 2, Table I). Instead of relying only on prominent gyri and sulci, this …”