Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns

“Based on its cytoarchitectonic structure, Petrides and Pandya (1999) separated the mid-dorsolateral prefrontal cortex from the posterior prefrontal cortex.”

“It has been argued previously (Petrides, 1991, 1994; Petrides and Pandya, 1999) that lesions limited to this part of the sulcus principalis, which receives primarily visual and somatosensory spatial input, might result in a purely spatial impairment (e.g., spatial delayed response tasks) and…”

“…of reciprocal corticocortical connections between regions in the PFC and VAC (Ungerleider et al. 1989; Webster et al. 1994; Barbas 2000; Petrides and Pandya 2002), including projections from the middle frontal gyrus (MFG; Petrides and Pandya 1999; Rempel- Clower and Barbas 2000; Blatt et al. 2003).”

“Massachusetts Institute of Technology To provide evidence for such a link, we examined the Cambridge, Massachusetts 02139 lateral PF cortex, a brain region that receives inputs from the IT cortex (Barbas and Mesulam, 1985; Pandya and Yeterian, 1990; Petrides and Pandya, 1999) and Summary plays a central role in behavi…”

“There was also enhanced activity in the temporal–spatial prediction task in the dorsolateral prefrontal cortex [area 46 (Petrides and Pandya, 1999)] and in the anterior presupplementary motor area.”

“, 2006] as well as to higher-order association areas in the prefrontal lobe [Petrides and Pandya, 1999].”

“The prefrontal cortex apparently uses these anatomical pathways for functional interactions to control the activities of cortical and subcortical structures.”

“…any gap; FOV = 128 3 96 mm; 128 3 96 matrix; 1.0 mm slice thickness; TR = 10000 ms; TE = 145 ms; 1 average; interleaved acquisition; two b-values of 0 and 1000 s/mm2; 1056 Hz/pixel bandwidth; image acquisition time of 5910$ for 29 directions and 5930$ for 31 directions for full 60 direction set].”

“The L-DLPFC was based on cytoarchitectonic features that included Brodmann areas 8A, 46, and 9/46, which have a well-developed layer IV (Petrides and Pandya, 1999; Petrides, 2005).”

“…connectivity between the ACC and frontal regions are consistent with anatomical evidence suggesting that the dorsolateral prefrontal and orbitofrontal cortices send to and receive dense projections from the ACC (Barbas, 1992; Petrides & Pandya, 1999), particularly area 24 and rostral area 32.”

“One additional confounding factor in such studies is that the DLPFC itself is a large region, heterogeneous in both its cytoarchitecture and anatomical connectivity to other regions[36–38].”

“In contrast, the dorsomedial and mid-dorsolateral PFC are highly connected in both humans and primates to regions associated with visuospatial and memory processes, such as the PCC and retrosplenial cortices, as well as areas of the superior temporal sulcus (STS) (Petrides and Pandya, 1999).”

“…cortex is a reasonable starting point because, generally speaking, these three cortical areas have different cytoarchitecture and different patterns of connectivity, both in humans (Petrides & Pandya, 1999, 2002) and in nonhuman primates (Barbas, 2000; Dombrowski, Hilgetag, & Barbas, 2001).”

“However, using AUT as experimental tasks, Kleibeuker et al. [2013] found that DLPFC (BA 6 or/and BA 9) is involved in generating creative ideas, whereas VLPFC is not.”

“S1D) is consistent with previous observations in patients with lateral prefrontal lesions (49), a metaanalysis of functional connectivity (50), the effect of DLPFC TMS on anterior cingulate blood flow (51), and with the description of anatomical connections in primates (46, 52).”

“A part of Broca's area (BA44/45) was also activated in the present study; this area may be the homologue of macaque premotor region F5, an intermediate level in the motor hierarchy receiving input from BA 9/46 (ref”

“Projections from the pre-SM A or PMdr to other motor-related areas (Barbas and Pandya, 1987; Luppino et al., 1993; Petrides and Pandya, 1999) and the brainstem reticular formation (Keizer and Kuypers, 1989) likely mediate these motor functions.”

“A statistically significant peak falls within a cluster of three left-lateralized activations that start in Brodmann’s area 8 and continue into Brodmann’s area 9 (Petrides and Pandya, 1999; Petrides, 2005).”

“The functional evidence for a frontocingulate network is supported by neuroanatomical findings showing that PFC projects to and receives information from ACC, particularly via association fibers in the cingulum bundle (Barbas, 1992; Petrides and Pandya, 1999).”

“…exteroceptive information, regions involved in cognitive processing, as well as portions of the basal ganglia that are linked to motivation (Balsters et al., 2016; Craig, 2009; Mesulam and Mufson, 1982; Neubert et al., 2015; Pandya et al., 1981; Petrides and Pandya, 2006; Vogt and Pandya, 1987).”

“The anterior cingulate cortex (ACC) and the superior and middle frontal gyri, which are parts of the dorsolateral prefrontal cortex (DLPFC, Brodmann’s areas 8, 9, 10, 46), were delineated as proposed by Mai et al. [26] and Petrides and Pandya [ 34 ] (Fig. 1a).”

“…major architectural fields can be used as a frame of reference for analysis of functional data in both monkey and human (Pandya & Yeterian 1996; Petrides & Pandya 1999, 2002), it is possible that these do not each correspond to an 'area', at least in the same way that V1 or MTare sharply…”

“…that injections of retrograde tracers in the mid-dorsolateral prefrontal cortex, but not in other prefrontal cortical areas, resulted in a signi®cant number of labelled neurons in the posterior cingulate cortical area 23 and the retrosplenial cortex (areas 30 and 29) (Petrides & Pandya, 1999).”

“The peaks of the SFG activations fall at the border between the rostral premotor cortex (BA8B) and a portion of the dlPFC (BA9), which is more cytoarchitectonically similar to BA8 than the rest of the dlPFC (BA46 and BA9/46) (Petrides and Pandya, 1999).”

“For instance, rTMS-induced excitation of prefrontal±temporal connections may have resulted in deactivation of mesial temporal areas which are strongly interconnected with the prefrontal cortex in monkeys (Petrides and Pandya, 1999; Thierry et al., 2000).”

“It tends to lie within the area identified anatomically as area 8 [9], and delay-related activity has also been reported in this area in monkeys (Figure 1; [10,11]).”

“For example, ACC and LPFC have stronger connections with motor areas than OFC and so may be more involved in encoding the physical costs associated with an outcome (Dum & Strick, 1993; Carmichael & Price, 1995; Petrides & Pandya, 1999).”

“The above findings strongly suggest that there is a homologous neurobiological substrate for working memory between the two species (Petrides and Pandya 1999; Petrides 2000; Nakahara et al. 2002; Rosano et al. 2002).”

“…posterior sensory regions all the way through to the prefrontal cortex (Arnott et al., 2004; Cohen et al., 2009; Goldman-Rakic, 1988; O’Reilly, 2010; Petrides & Pandya, 1999, 2001, 2006, 2007; Romanski, Bates, et al., 1999; Romanski, Tian, et al., 1999; Wilson, O’Scalaidhe, & Goldman-Rakic, 1993;…”

“We aimed to use unambiguous sulcal landmarks that are reliably visible on MRI scans in order to define the regions that have been hypothesized (Petrides and Pandya, 1994, 1999, 2002), on the basis of cytoarchitectonic considerations, to correspond to the macaque regions of interest.”

“…somatosensory, and auditory areas and receives the information from occipital, parietal, and temporal cortices and is shown to be important in several cognitive functions, including executive function (Chand and Dhamala, 2017; Chand et al., 2016; Miller and Cohen, 2001; Petrides and Pandya, 1999).”

“Cortico–cortical connections preferentially link the DLPFCd and DLPFCv with the PMd and PMv, respectively (Barbas and Pandya 1987; Luppino et al. 2003; Petrides and Pandya 1999, 2002; Wang et al. 2002).”

“This pattern of cortical connectivity is consistent with that described by Petrides and Pandya (1999) for area 8Ad in the macaque.”

“As far as we know, the RLPFC interacts primarily with other PFC subregions, rather than with the posterior cortical regions implicated in long-term memory representation (Ramnani & Owen, 2004; Petrides & Pandya, 1999).”

“It projects to secondary motor regions (Petrides & Pandya 1999), the basal ganglia (Nambu 2008), and the ACC and VMPFC (McDonald et al. 1996).”

“The extent to which the subregions defined here correspond to distinctive functional modules may be debatable; however, current views on gyralfunctional correlations (Geyer et al., 1999, 2000; Petrides and Pandya, 1999) as well as previous efforts utilizing similar Brodmann-based boundaries for cortical parcellation (…”

“Furthermore, reciprocal connections of the ACC and lateral prefrontal cortex (LPFC) have been described (Petrides & Pandya, 1999; Bates & GoldmanRakic, 1993).”

“Areas 9 and 46 are primarily connected to other regions of prefrontal cortex, both within areas 9 and 46 and with areas 8A (including the frontal eye field; FEF), 32 and 24b (Barbas, 1992; Carmichael & Price, 1996; Petrides & Pandya, 1999).”

“The prefrontal cortex (A9) is the target of massive intra-and subcortical afferents from almost all sensory modalities, motor cortex and thalamus (Middleton and Strick, 2002; Petrides and Pandya, 1999).”

“The DLPFCd includes the dorsal part of area 46, area 9/46d, and the rostral part of area 8Ad (Petrides and Pandya, 1999), and the DLPFCv includes the ventral part of area 46, area 9/46v, and the rostral parts of areas 8Av and 45 (Petrides and Pandya, 1999).”

“Three prefrontal cortex sectors were identified as regions of interest and were quantified by using ABLe: 1) the ventromedial/orbitofrontal cortex (Brodmann’s area 25, lower 24, 32, medial aspect of 11, 12, and 10, and 13, 14, 47) (34–36), 2) the dorsolateral prefrontal cortex (Brodmann’s area 9/46) (37), and 3) the a…”

“The DLPFC has reciprocal connections with ACC (Paus, Castro-Alamancos, & Petrides, 2001), the inferior parietal cortex, the SMA, the pre-SMA, and the premotor cortex (Ridderinkhof, van den Wildenberg, Segalowitz, & Carter, 2004; Paus et al., 2001; Koski & Paus, 2000; Petrides & Pandya, 1999).”

“There are also connections via the arcuate fasciculus (AF) (or superior longitudinal fasciculus) between the DLPFC and the STG and temporal association cortex (Ban et al. 1991; Petrides & Pandya 1988; 1999).”

“…1987) STR → CSr (Alexander et al., 1986; Ilinsky and Kultas-Ilinsky, 1987) IFS → IFG (Barbas and Pandya, 1989; Petrides and Pandya, 1999) IFG → IFS (Barbas and Pandya, 1989; Petrides and Pandya, 1999) IPS → PCd (Cavada and Goldman-Rakic, 1989; Matelli et al., 1998) IPS → IFS (Cavada and…”

“On the basis of this evidence, the anatomical connectivity of the OFC (Petrides & Pandya, 1999; Price, 2006), and studies showing impairments in simple economic choice tasks in patients with lesions to this area (Fellows & Farah, 2007), it has been suggested that the OFC might be an area where…”

“The cytoarchitecture of the PMC, DLPFC and ACC was identi®ed according to well-de®ned microscopic criteria, as described by Brodal (1992), Petrides and Pandya (1999) and Vogt et al. (1995), respectively.”

“Prefrontal activations were found bilaterally in the middle frontal gyrus (in the region of areas 9/46 of Petrides and Pandya, 1999) and the anterior cingulate cortex (putatively BA32; see Fig.”

“Petrides and Pandya (1999, 2002, 2006, 2007), in particular, have approached this topic with several studies of the efferent (or afferent) connections of the dorsomedial, ventrolateral, caudal, and rostral parts of the LPFC. Based on these studies, Pandya and his colleagues have proposed that the…”

“The neurolinguistic test battery consisted of Part B of Bilingual Aphasia Tests (BAT) (Bilingual Aphasia Test, Paradis, 1987) for Italian and Spanish and the Snodgrass Naming battery (Snodgrass, 1980).”

“However, there were significant differences in the effects of rTMS on spatial and face stimuli following rTMS to the VPFC [F(1,21) = 6.97, P < 0.02].”

“Anatomically, the PFC is in an advantageous position to contribute to reasoning through integrating relational information, as PFC subregions are densely interconnected and it has reciprocal connections with multiple other brain areas (Petrides and Pandya, 1999).”

“…in nonhuman primates have reported distinct areas in lateral frontal cortex that are biased toward audition or vision in anatomical connectivity and/or functional response (for example, see Barbas and Mesulam , 1981; Petrides and Pandya, 1999; Romanski and Goldman- Rakic, 2002; Romanski, 2007).”

“Such problems require extensive model variation and we found increased activation in the rostral DLPFC, corresponding to BA 9.”

“However, the exact positions of areas 44 and 45 were anatomically not verified until recently [57,78].”

“In our study, however, anterograde tract-tracing data do not agree with such a result, because only rarely was terminal labeling observed in area 46 after tracer injections into the CMAs (see also Petrides and Pandya, 1999).”

“A possible explanation for this is that the inactivated sites corresponded to areas 46 and 9/46 (Petrides and Pandya, 1999), whereas our corticotectal neurons were recorded primarily from area 8a, anterior to FEFs.”