Forward frontal fields: phylogeny and fundamental function

“They contribute to prospective coding[41,42]; sensory working memory[43,44]; attention to objects, places, actions and intentions[36, 45 ,46]; response inhibition[47]; the categorization of objects, sounds and event sequences[48‐50]; the selection, generation and sequencing of multiple actions[51‐53]; problemsolving s…”

“Research on the ‘granular’ prefrontal cortex of humans emphasizes such processes as updating, manipulating and strategic controlofinformationstoredinshort-termmemory[33, 67 ]; establishingtasksetsandrules[68];mediatinghierarchies of behavioral control; behavioral inhibition; cognitive control in social situations[69];…”

“Neurophysiological results that had been interpreted as memory signals[ 35 ]enabled other interpretations, usually because crucial variables remained uncontrolled and often unmonitored.”

“The idea that the knowledge stored by the ‘granular’ prefrontal cortex concerns aspects of behavior agrees with previous proposals about its role in behavioral flexibility and the diversity of its cognitive contributions, as propounded for example by Duncan and colleagues[72, 73 ,75]and by Shallice and Norman[76,77]as…”

“They contribute to prospective coding[41,42]; sensory working memory[ 43 ,44]; attention to objects, places, actions and intentions[36,45,46]; response inhibition[47]; the categorization of objects, sounds and event sequences[48‐50]; the selection, generation and sequencing of multiple actions[51‐53]; problemsolving s…”

“The idea that the knowledge stored by the ‘granular’ prefrontal cortex concerns aspects of behavior agrees with previous proposals about its role in behavioral flexibility and the diversity of its cognitive contributions, as propounded for example by Duncan and colleagues[72,73,75]and by Shallice and Norman[ 76 ,77]as…”

“They contribute to prospective coding[41,42]; sensory working memory[43,44]; attention to objects, places, actions and intentions[36,45, 46 ]; response inhibition[47]; the categorization of objects, sounds and event sequences[48‐50]; the selection, generation and sequencing of multiple actions[51‐53]; problemsolving s…”

“In addition, rat mPFC, similar to its putative functional analog primate dorsolateral prefrontal cortex (e.g., Brown and Bowman, 2002; Wise, 2008; but see Vogt and Paxinos, 2014), has neuronal firing patterns that distinguish contexts (Hyman et al., 2012; Mante et al., 2013), and mPFC neurons…”

“…agree that rodents lack a cortical region homologous to primate dorsolateral PFC, there is a widespread consensus that rodents and primates possess functionally analogous medial and orbital prefrontal cortical areas (Brown & Bowman 2002; Ongür & Price 2000; Preuss 1995; Wallis 2011; Wise 2008).”

“There may be no cortical area in rodents that is homologous to most of the primate including human orbitofrontal cortex (Wise 2008).”

“The homologies in cortical areas across species in the evolutionary tree, based on both cytoarchitectonics or connectome and sensorimotor or cognitive tests, are still debated (22).”

“First, the rodent data involve lesions of an orbitofrontal area that is not homologous with the part of the PFo studied here (Wise, 2008).”

“Third, the orbitofrontal cortex is very little developed in rodents (with only an agranular part) (183), yet it is one of the major brain areas involved in taste and olfactory processing, and emotion and motivation, in primates including humans (114).”

“Lesions were primarily constrained to rodent Cg1 and showed little overlap with other frontal regions (35).”

“There may also be heterogeneity in the area along the anterior-posterior axis in rodent brains (Wise, 2008).”

“Rodents lack homotypical frontal areas, and the areas called orbitofrontal cortex in rodents are poor candidates for homologues of any homotypical prefrontal area in primates, including the parts of PFo studied here (Preuss, 1995, 2007; Wise, 2008).”

“Based on this cytoarchitectonic evidence, it has been suggested recently that the rat OFC may be a model to study the function of the agranular most caudal region of monkey OFC (Wise, 2008), which receives inputs from olfactory and gustatory cortices (Cavada et al., 2000).”

“Whether, there is a homolog for the primate LPFC in the mouse or rat has been a matter of some discussion and debate (Preuss, 1995; Uylings et al., 2003; Kolb, 2007; Wise, 2008; Van De Werd et al., 2010; Barbas, 2015).”

“In terms of cytoarchitecture, the human OFC comprises an anterior granular cortex and a posterior agranular cortex, which are distinguished on the basis of the presence or absence of small and round neurons in layer IV (Wise, 2008; Wallis, 2012).”

“Fr2 has been compared to the frontal cortex of primates, although there is debate concerning the precise mapping of homologous primate and rodent frontal regions(Preuss, 1995; Uylings et al. , 2003; Wise, 2008).”

“, 2007; Preuss, 2007), which endow the two species with a shared repertoire of complex social, emotional, and cognitive behaviors (Belmonte et al., 2015; Kalin & Shelton, 2003; Preuss, 2007; Wise, 2008).”

“Based on the phylogenetics and ontogenesis of the prefrontal cortex (PFC) (Semendeferi et al., 2001; Wise, 2008), it is posited that reward stimuli that are more complex and abstract depend on the more anterior mPFC, whereas reward stimuli that are more basic or tangible depend on the more posterior mPFC (Kringelbach…”

“That is, ventromedial PFC is densely interconnected with the rostral anterior cingulate area (Brodmann Area 32) that is the hypothesized homologue of rodent prelimibic cortex (Wise, 2008).”

“As the PFC expands greatly in primates (Wise, 2008), these actions are particularly important in these higher species, and may be why α2A-AR agonist pro-cognitive effects were initially discovered in monkeys.”

“MRI studies of individuals with AS point to changes in gray mater volume of orbitofrontal areas (Aghakhanyan et al., 2016), which is homologous to the rodent mPFC (Wise, 2008; Balleine and O’Doherty, 2010).”

“Consistent with a role in advanced cognition, the areas composing PFg are primate innovations, whereas most if not all mammals share the agranular frontal areas mentioned above [59].”

“Since rodent OFC is entirely agranular, one proposal is that the discrete regions are likely to be most similar to those agranular regions located in caudal aspects of primate OFC (Wise, 2008).”

“One problem is that although the MD-projection cortex and granular cortex overlap, the MD-projection cortex extends well beyond the granular regions in primates (see Wise, 2008).”

“Monkeys arguably provide the best model of human brain function related to psychiatric disorders because of similarities in brain structure, social organization, and protracted development (13).”

“many of them to date, however, remains unclear (4).”

“…massive backprojections from parts of the brain where mood is represented, such as the OFC and amygdala, to the cortical areas such as the inferior temporal visual cortex and hippocampus-related areas (labeled IT in Figure 8) that project into these mood-representing areas (Amaral et al., 1992).”

“There is a longstanding controversy surrounding the designation of the PFC in the rodent and whether it is truly homologous to the PFC in the primate (Preuss, 1995; Uylings et al., 2003; Kolb, 2006; Wise, 2008; Carlén, 2017).”

“rat dmPFC bears functional similarities to primate dorsolateral PFC (Uylings, Groenewegen, & Kolb, 2003) but also shares anatomic features with primate orbitomedial PFC (Heilbronner, RodriguezRomaguera, Quirk, Groenewegen, & Haber, 2016; Preuss, 1995; Wise, 2008).”

“The rodent prelimbic cortex (Figure 1) seems homologous to human BA 32 that is part of the dorsal and ventral PFC, including the lateral PFC (96, 101).”

“In contrast, the similarity between the PFC of rodents and primates has been historically controversial (Preuss, 1995; Uylings et al., 2003; Wise, 2008; Brodmann, 1909; Rose and Woolsey, 1948).”

“Cognitive constructs such as impulsivity, compulsivity and flexibility are closely interrelated executive processes in the context of inhibitory control, hierarchically top-down mediated by the PFC [69,70].”

“(2) The prefrontal cortex is a crucial part of the frontal lobe and has been found to be implicated in different higher-order cognitive and executive functions (e.g. working memory, spatial attention, etc.) in humans (Wise, 2008; Arnsten et al., 2012; Vijayraghavan et al., 2017).”

“cialization of the primate order and cannot be identified in rodent species (Carlén, 2017; Wise, 2008).”

“great apes and humans) [4,10,27,64,65,66,67,68,69,70].”

“…in this context, the primate including the human orbitofrontal cortex is very greatly developed compared to what is present in rodents (Preuss 1995; Wise 2008; Passingham and Wise 2012; Rolls 2019b; Rolls et al. 2020b; Rolls 2021a), and indeed rodents are not known to be able to perform one-trial…”

“…regulation by the PFC provides perspective, insight and optimism, helping us persevere through challenges (Aziz-Zadeh et al., 2009; Dolcos et al., 2016; Hecht, 2013; Hilgenstock et al., 2014; Kuzmanovic et al., 2018; Sharot et al., 2007; Szczepanski and Knight, 2014; Wise, 2008; Wu et al., 2015).”

“…neural activity following acute ketamine administration (Jackson et al., 2004; Homayoun and Moghaddam, 2007), rodents lack a granular PFC, which is characteristic for lateral, ventral, medial, and frontopolar prefrontal areas in primates (Povinelli and Preuss, 1995; Preuss, 2000; Wise, 2008).”

“In cocaine-extinguished animals, cues induced c-fos mRNA and Fos protein expression in the PFC, VTA, dorsal striatum, and NAc.”

“Lateral prefrontal cortex is another key node (Barraclough et al. 2004a; Genovesio et al. 2005; Wise 2008) that mediates flexible behaviors using information about available options, current context, and the outcomes of previous actions obtained through the interactions with the anterior cingulate…”

“Although rodents lack a granular prefrontal cortical region comparable with that of primates (Wise, 2008), it is generally agreed upon that the rodent mPFC performs working memory functions analogous to those subserved by dorsolateral area 46 in the primate prefrontal cortex (Brown and Bowman,…”

“, 2018), which is not surprising given the enormous species differences spanning from brain anatomy (Wise, 2008) to molecular isoforms and splicing variants (Leung et al.”

“The rodent mPFC is implicated in a wide array of higher cognitive functions that are analogous to the primate prefrontal cortex (Wise, 2008), including decision-making, working memory, and perceptual set-shifting (Arnsten et al., 2010; Brown and Bowman, 2002; Divac, 1971; Otto and Eichenbaum,…”

“…of an animal’s threat responsiveness (Figure 2a), regardless of whether the interventions are excitotoxic lesions of agranular insula (AI)/DLO, LO (Lacroix et al. 2000, Zelinski et al. 2010), DLO (Ray et al. 2018), or LO-VO (Costanzi et al. 2014), or inactivation of LO (Sarlitto et al. 2018).”

“Cross-species comparisons of connectivity suggest that rodent mOFC is homologous to the medial region of the OFC in humans (Brodmann area 14) (Price, 2007; Wallis, 2012; Wise, 2008).”

“Importantly, while the macaque frontal lobe is certainly not a “minia- turized” human frontal lobe, the two display similar prefrontal maps of agranular and granular cortex, the latter of which is completely absent from the rodent frontal area (Preuss, 1995; Wise, 2008).”

“Rather than center our analysis on the evolution of neuroanatomy (which can be found in Preuss and Wise, in this issue) or evolution more generally [5], here we focus on cytoarchitecture and the connections of frontal cortex.”

“Interestingly, in primates and particularly in humans, the evolutionarily newer far-anterior frontal areas, rostral to primary motor areas, do possess a more distinct granular L4 (Wise, 2008).”

“PFC is also connected with which regions known as social brain, so PFC has been played rol in also social behavior [119, 120].”

“The prefrontal cortex in rodents encompasses the agranular insular cortex, the orbitofrontal cortices and some of the cingulate cortices [49].”

“These studies provided crucial contributions to clarify both the mechanisms underlying PFC executive functions and the possible evolutionary trends leading to the origin of uniquely human cognitive capacities (Wise, 2008; Genovesio et al., 2014).”

“The other dopamine projection originating from the substantia nigra projects to dlPFC (BA 12/47 and BA9/46) (Wise, 2008).”

“We established that, as was described previously (Ongür and Price, 2000; Wise, 2008; Vogt and Paxinos, 2014), IL in rodents and area 25 in primates are homologous (Heilbronner et al., 2016).”

“The bidirectional connectivity between mPFC and BF has attracted great interest as a circuit involved in modulating decision making, cortical arousal, and learning and memory (Groenewegen and Uylings, 2000; Miller and Cohen, 2001; Dalley et al., 2004; Henny and Jones, 2008; Wise, 2008; Ramanathan et al., 2009; Martino…”

“There is a general agreement in the role of the prefrontal cortex in decision-making (DM), under conditions of complexity and unpredictability (e.g., Bechara et al., 2000a; Bechara, 2001; Clark et al., 2003; Wise, 2008; Gläscher et al., 2012).”

“Most recordings from OFC in primates focus on areas 11 and 13, dysgranular cortex that may not have a homolog in rodents (Wise, 2008).”

“For example, the frontal cortical area in mice implicated in attentional control, speci fi cally anterior cingulate cortex (ACC) [36,66], is likely not anatomically homologous with dlPFC in primates, and instead may be homologous with primate medial prefrontal (mPFC) areas [71].”

“The prefrontal cortex has no clear structural or functional homolog in rodents [1 ,3], which suggests advantages of using non-human primates to model human neurological and psychiatric diseases.”

“While there are major differences in prefrontal anatomy between the human, non- human primate, and rodent brain (Heilbronner et al., 2016; Laubach et al., 2018; Wise, 2008), studies in laboratory animals have been valuable in helping define the roles of cortical structures to risky decision making.”

“Wise (2008) argued in his review comparing the frontal cortices of primates and rodents that there is no brain region in the rodent frontal cortex that is comparable to the primate PFC, referring to the conventional anatomical definition of the primate PFC as the frontal ‘‘granular’’ cortex, which…”