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…”

“Furthermore, medial MOs contains features similar to those found in the supplementary motor cortex, premotor cortex, and frontal eye field of primates (Barthas & Kwan, 2017; Wise, 2008).”

“It has been proosed that the rodent prelimbic cortex is homologuous to BA 32, nd thus corresponds to the human mPFC/vmPFC (Wise, 2008).”

“Disentangling the contributions of sensorimotor and cognitive variables to NCL neural responses will be crucial to further constrain hypotheses on the precise function of this structure as well as its relation to subdivisions of the mammalian PFC (Wise, 2008; Herold et al., 2011).”

“The prefrontal cortex (PFC) is a critical node in brain networks involved in complex cognitive functions and has undergone a great evolutionary expansion in primates (Wise, 2008).”

“mulatta) was selected because of its similarity to humans in the gross organization of the frontal lobes (Wise, 2008), cortical distribution of dopaminergic terminals (Berger et al.”

“This may be particularly true between rodents and non-human primates or humans (Wise, 2008), as the latter two display high anatomical and functional homology in terms of brain areas related to reward-guided learning and decisions (Neubert et al., 2015).”

“Examining these cortico‐striosomal circuits in non‐human primates, therefore, has special value (Wise, 2008), as their decision‐related circuitry is considered to be more nearly homologous to cortical regions that in humans (Neubert, Mars, Sallet, & Rushworth, 2015) are implicated in neuropsychiatric disorders (Pizzag…”

“Wise (2008) espoused a similar view that he vividly summarised as follows: ‘The long list of functions often attributed to prefrontal cortex may all contribute to knowing what to do and what will happen when rare risks arise or outstanding opportunities knock’ (p. 599).”

“regions referred to as OFC in rodents and new-world monkeys have similarities with the posterior OFC and adjacent AI of old-world primates such as macaques [22,23].”

“For instance, as mammals all primates share a six-layered neocortex as endbrain integration center, but also a primate-specific granular dorsolateral prefrontal cortex [9].”

“NHPs share with humans many brain regions, circuits, and cell types critical for higher cognitive capacity [5].”

“In particular, neurons in the lateral prefrontal cortex (lPFC) are known to dynamically represent context- and goal-relevant rules and behavioral repertoires, which can bias processing in distal regions to promote context-appropriate behavior (Miller & Cohen, 2001; Sakai & Passingham, 2006; Wise, 2008).”

“As primates, marmosets share characteristic features of the human brain (e.g., highly granular frontal lobe, expanded temporal lobe), offering a distinct advantage over rodent models (Homman-Ludiye and Bourne 2017; Izpisua Belmonte et al. 2015; Mitchell and Leopold 2015; Wise 2008).”

“Cognitive constructs such as impulsivity and behavioural flexibility are closely interrelated executive processes in the context of inhibitory control, hierarchically topdown, mediated by the PFC (Bari and Robbins 2013; Wise 2008).”

“Especially the human prefrontal cortex is more advanced and the existence of a convincing rodent homologue is still under debate [33, 34].”

“Structurally, the PFC in rodents lacks the granular layer (layer IV) characteristic of the primate PFC, making it entirely agranular [4].”

“T dorsolateral PFC (DLPFC) [20].”

“…representational approach is more general (since the characterization of the kind of processes that PFC stores fits it), more in line with evolutionary history of PFC and its anatomical properties (see also Wise, 2008) and potentially more fruitful in generating experimentally testable predictions.”

“and Wise, S. P. (2012). The Neurobiology of the Prefrontal Cortex, Oxford University Press, Oxford.”

“The amygdala has evolutionarily old origins and can be identified, as can the hippocampus, in amphibia (Isaacson, 1982; Medina et al., 2011), whereas most of the orbitofrontal cortex, the granular parts, is new to primates (Wise, 2008; Passingham and Wise, 2012; Fig.”

“…omnivorous diet that might provide a selective advantage for the seeking of new outcomes of foraging choices or the heightened conspecific competition in a rigidly hierarchical social system (Thierry et al., 2004; Evans and Beran, 2007; Wise, 2008; Kralik et al., 2012; Passingham and Wise, 2012).”

“In rodents, hippocampal subfield CA1 has a strong unidirectional projection with the medial PFC (“mPFC” Thierry, Gioanni, Degenetais, & Glowinski, 2000), which may be relatively homologous to “agranular” prefrontal areas in humans, including the subgenual anterior cingulate cortex and/or ventromedial PFC in humans (Wi…”

“Further evidence that the vmFL is not a single entity is a result of neuroanatomical evidence delineating granular and agranular subregions within the vmFL (Barbas & Garcia-Cabezas, 2016; Henssen et al., 2016; Wise, 2008).”

“These regions are well represented in the macaque brain, but not present or only rudimentarily defined in the primary animal model i.e. the rodent brain (Preuss, 1995; Willard et al., 2015; Wise, 2008).”

“The macaque areas 24/32 are considered to be homologous to the human areas 24/32 (Adapted from Wise, 2008).”

“Participation in experimental sessions and the execution of complex tasks, such as the memory-guided saccade, require the contribution of various cognitive/behavioral functions, which can be difficult to differentiate (Wise, 2008).”

“For example, primates can flexibly combine individual cues across extended periods of time to construct goal- directed behaviour (Passingham & Wise, 2012).”

“Rodent models of PFC cognitive disorders have focused on the mPFC, as rodents do not have dlPFC (Wise, 2008), and the mPFC shares some key characteristics with primate dlPFC.”

“Notably, several of these “intermediate interface” areas in primates are agranular, which have been proposed to be the most likely homologs with rodent agranular OFC regions (Wise, 2008).”

“Many of the areas that form the MDN are regions that evolved or expanded in primates, such as posterior parietal cortex (Goldring and Krubitzer 2017) and parts of prefrontal cortex (Wise 2008; Passingham 2021).”

“1 decision-making, goal-directed behavior and emotion (Groenewegen and Uylings, 2000; Miller and Cohen, 2001; Dalley et al., 2004; Wise, 2008).”

“The PFC is significantly larger in humans, compared to rodents, due to the developmental expansion of the dorsolateral PFC and the frontal pole, seen in primates, but absent in rodents (Wise, 2008).”

“When drawing comparisons between human and rodent work on the PFC, it is important to consider that, as the prefrontal cortex is considerably larger and shows a commensurate increase in the number of subregions in primates compared to rodents (Wise, 2008), it is difficult to create one-to-one comparisons between roden…”

“While it is certainly possible that this discrepancy could be chalked up to species-specific differences in brain architecture [14], and/or differences in task design, the study reported in this issue of PLOS Biology by Strait and colleagues [15] argues against these interpretations.”

“Although the mouse frontal cortex is simpler than that of the primate, it contains evolutionarily conserved circuit architecture for top-down control of somatomotor and visceromotor functions, including convergent multisensory inputs, recurrent local connections and strong dopaminergic (DA) neuromodulation (Wise, 2008…”

“…exploration (Barton, 1998), an expanded association cortex, including prefrontal association cortex, enabling high levels of cognitive control (Wise, 2008, Smaers J et al., 2008), (Roberts and Clarke (2019) and a primate-specific motor system with direct pyramidal tract connections enabling…”

“Studies on non‐primate animal models have postulated that prefrontal areas (as a functional block) are not unique to primates, although this idea continues to be controversial (Uylings, Groenewegen, & Kolb, 2003; Wise, 2008).”

“In particular, brain structures associated with higher cognition (e.g., frontal cortex) are larger and more complex in NHPs. Parts of these structures are implicated in psychiatric disorders and may have no homolog in other mammals (Wise, 2008).”

“Whereas patent homologies exist between human and nonhuman primates for the most recently evolved regions of the brain (Wise, 2008), many neural structures that we can study in detail in macaque monkeys have not been identified conclusively in nonprimates, and many of them do not exist – particularly the granular PFc…”

“Interestingly, the rodent IL and corresponding human Brodman area 25 are thought to exert important functions in fear extinction, habitual behaviours and memory consolidation [9, 20, 22].”

“…used non-human primate species for studying higher-order cognition due to their having similar brain organisation to humans (see Preuss, 1995; Wise, 2008), and their ability to perform highly complex cognitive tasks most like those used in human neuropsychological research (e.g., the…”

“The DLPFC plays a key role in specific mechanisms of cognitive control and behavior (Wise, 2008; Friedman and Robbins, 2022), which includes executive functions, such as monitoring (O’Reilly, 2010), controlling behavioral strategies (Shallice and Burgess, 1991; Barraclough et al.”

“TheseMFC brain regions include the anterior cingulate cortex (ACC), dorsal, medial, and ventral sub-divisions of the medial prefrontal cortex (mPFC), supplemental motor area (SMA), pre-SMA, as well as the medial aspects of the orbitofrontal cortex (OFC), among others (Wise, 2008).”

“cortex) shares similarities with rat prelimbic cortex (Wise, 2008; Balleine & O’Doherty, 2010).”

“Rhesus monkeys were selected because they are the animal preparation with the closest homolog to the human frontal brain available for studies of this type (Wise 2008).”

“This problem is compounded by the neocortical expansion of the primate brain [32].”

“…that the micro-anatomical structure of the human prefrontal cortex © 2011 The Author Educational Philosophy and Theory © 2011 Philosophy of Education Society of Australasia cannot be found in rodents (Wise, 2008), and be careful in applying conclusions drawn from rodent-based studies to humans.”

“…brain d Biob a s h t fi e e i i i A b s w 2 t N i ( N a c n w L 2 t l u s p n S c i v i t i 2 o o t u d p p s t i a o s s A p p a m w f W a E. Monfardini et al. / Neuroscience an reas that appeared with primate evolution and underlie the outtanding flexibility of primate behavior (Wise, 2008).”

“2, there may be no cortical area in rodents that is homologous to most of the primate including human orbitofrontal cortex (Preuss, 1995; Wise, 2008; Passingham and Wise, 2012).”