Expression of m1‐type muscarinic acetylcholine receptors by parvalbumin‐immunoreactive neurons in the primary visual cortex: A comparative study of rat, guinea pig, ferret, macaque, and human

“V1 was identified in all species by using Nissl-stained reference sections, aided by brain atlases and published data (Choudhury, 1978; McConnell and LeVay, 1986; Paxinos and Franklin, 2003; Paxinos et al., 2000; Paxinos and Watson, 2007; White et al., 1999).”

“…intestinal peptide-ir neurons are depolarized by muscarine (Kawaguchi, 1997), and neurons such as bipolar and bitufted inhibitory neurons, which can express cholecystokinin or vasoactive intestinal peptide, can also often express calbindin or calretinin (reviewed by Markram et al., 2004).”

“When expressed by excitatory neurons, m1 AChRs couple to the m-current (Brown and Adams, 1980), a potassium current that underlies spike frequency adaption.”

“Evidence for ACh’s role in attention arises from studies of both species (Deco and Thiele, 2011; Herrero et al., 2008; Sarter et al., 2005).”

“The authors did not stain for PV in these fast-spiking neurons, but given their physiological properties it is likely that they were PV-ir neurons (Kawaguchi and Kubota, 1993).”

“Despite the different anatomical circuits, ACh is suppressive in the rodent cortex (Gil et al., 1997; Hasselmo and Bower, 1992; Hsieh et al., 2000; Kimura, 2000), as it is in the macaque cortex (Disney et al., 2012), and ACh has been shown to boost thalamic gain in both species (Disney et al.,…”

“It has been proposed by numerous investigators that cortical cholinergic modulation underlies attention (Arnold et al., 2002; Deco and Thiele, 2011; Hasselmo and McGaughy, 2004; Herrero et al., 2008; Himmelheber et al., 2000; McGaughy and Sarter, 1998; Sarter et al., 2005), and it has also been…”

“This contrasts with PV expression in macaque prefrontal cortex and in the rodent neocortex, where only 50% of GABAergic neurons express PV (Conde et al., 1994; Gonchar and Burkhalter, 1997).”

“These data largely agree with the results of physiological studies that have reported profound effects of cholinergic modulation on PV neurons in guinea pigs (McCormick and Prince, 1986) but not in rats (Gulledge et al., 2007; Kawaguchi, 1997).”

“This contrasts with PV expression in macaque prefrontal cortex and in the rodent neocortex, where only 50% of GABAergic neurons express PV (Conde et al., 1994; Gonchar and Burkhalter, 1997).”

“…investigators that cortical cholinergic modulation underlies attention (Arnold et al., 2002; Deco and Thiele, 2011; Hasselmo and McGaughy, 2004; Herrero et al., 2008; Himmelheber et al., 2000; McGaughy and Sarter, 1998; Sarter et al., 2005), and it has also been argued that changes in…”

“It should be noted here that muscarinic receptor-mediated polarization changes in PV-ir neurons were reported in one previous in vitro study of layer 5 neurons in rat V1 (Xiang et al., 1998); these conflicting studies are discussed further below.”

“Following this incubation and after three 5- minute rinses in PBS, the sections were incubated in the Vectastain Elite ABC Kit (Vector) at room temperature on a shaker for 30–60 minutes.”

“…TERMS: striate cortex; neuromodulation; quantitative; anatomy; immunofluorescence; calcium-binding proteins; parvalbumin Neuromodulation of neocortical circuits by acetylcholine (ACh) is a candidate mechanism for aspects of arousal and attention in mammals (Muir et al., 1994; Sarter et al., 2005).”

“V1 also has a higher density of cell bodies in all primates than do other cortical areas (Collins et al., 2010) as well as smaller dendritic fields and a lower density of spines (Elston and Rosa, 1997).”

“Brightness and contrast settings were chosen by using a live color image.”

“…(Gil et al., 1997; Hasselmo and Bower, 1992; Hsieh et al., 2000; Kimura, 2000), as it is in the macaque cortex (Disney et al., 2012), and ACh has been shown to boost thalamic gain in both species (Disney et al., 2007; Gil et al., 1997; Hasselmo and Bower, 1992; Hsieh et al., 2000; Kimura, 2000).”

“For example, throughout the rest of the macaque neocortex, GABAergic interneurons comprise approximately 25% of the neuronal population, compared with only 20% in V1 (Beaulieu et al., 1992) and the composition of that population also differs from nearby visual areas (DeFelipe et al., 1999).”

“…cortical cholinergic modulation underlies attention (Arnold et al., 2002; Deco and Thiele, 2011; Hasselmo and McGaughy, 2004; Herrero et al., 2008; Himmelheber et al., 2000; McGaughy and Sarter, 1998; Sarter et al., 2005), and it has also been argued that changes in GABAergic inhibition could…”

“V1 also has a higher density of cell bodies in all primates than do other cortical areas (Collins et al., 2010) as well as smaller dendritic fields and a lower density of spines (Elston and Rosa, 1997).”

“It has been shown previously that ACh, acting via m2 AChRs does modulate GABA release by PV cells (Kruglikov and Rudy, 2008).”

“Sections for each species were always coprocessed with tissue from at least one other species (usually three or four species per processing “batch,” a batch being the sections in a single well).”

“…2011; Hasselmo and McGaughy, 2004; Herrero et al., 2008; Himmelheber et al., 2000; McGaughy and Sarter, 1998; Sarter et al., 2005), and it has also been argued that changes in GABAergic inhibition could account for response gain changes seen in V1 during attention tasks (Katzner et al., 2011).”

“This can result in undetectable somatic immunoreactivity in a neuron that actually expresses a protein of interest (Burette et al., 2002).”

“It has been proposed by numerous investigators that cortical cholinergic modulation underlies attention (Arnold et al., 2002; Deco and Thiele, 2011; Hasselmo and McGaughy, 2004; Herrero et al., 2008; Himmelheber et al., 2000; McGaughy and Sarter, 1998; Sarter et al., 2005), and it has also been…”

“In contrast, previous physiological data suggest that PV-ir neurons in the neocortex of rats rarely express pirenzepine-sensitive muscarinic AChRs (Gulledge et al., 2007; Kawaguchi, 1997; Kruglikov and Rudy, 2008).”

“Despite the different anatomical circuits, ACh is suppressive in the rodent cortex (Gil et al., 1997; Hasselmo and Bower, 1992; Hsieh et al., 2000; Kimura, 2000), as it is in the macaque cortex (Disney et al., 2012), and ACh has been shown to boost thalamic gain in both species (Disney et al.,…”

“…to problems of antibody specificity), but a recent study shows that in the mouse visual cortex in vivo ACh released as a result of basal forebrain stimulation activates 25% of PV neurons, via muscarinic receptors, when the surrounding cortex is only weakly desynchronized (Alitto and Dan, 2012).”

“…underlies attention (Arnold et al., 2002; Deco and Thiele, 2011; Hasselmo and McGaughy, 2004; Herrero et al., 2008; Himmelheber et al., 2000; McGaughy and Sarter, 1998; Sarter et al., 2005), and it has also been argued that changes in GABAergic inhibition could account for response gain…”

“In the neocortex, ACh is usually released from varicosities that are not apposed to a synaptic specialization (Aoki and Kabak, 1992; Beaulieu and Somogyi, 1991; Umbriaco et al., 1994), a mode of release known as volume transmission (but see Turrini et al., 2001).”

“In the neocortex, ACh is usually released from varicosities that are not apposed to a synaptic specialization (Aoki and Kabak, 1992; Beaulieu and Somogyi, 1991; Umbriaco et al., 1994), a mode of release known as volume transmission (but see Turrini et al., 2001).”

“We have shown previously, by electron micros- copy, that m1 AChRs are rarely expressed in distal processes (dendrites or axons) of any neurons in V1 of the macaque (Disney and Aoki, 2008; Disney et al., 2006).”

“We have shown previously, by electron micros- copy, that m1 AChRs are rarely expressed in distal processes (dendrites or axons) of any neurons in V1 of the macaque (Disney and Aoki, 2008; Disney et al., 2006).”

“Despite the different anatomical circuits, ACh is suppressive in the rodent cortex (Gil et al., 1997; Hasselmo and Bower, 1992; Hsieh et al., 2000; Kimura, 2000), as it is in the macaque cortex (Disney et al., 2012), and ACh has been shown to boost thalamic gain in both species (Disney et al.,…”

“Our finding that inhibition is a primary target for modulation of visual processing by ACh in macaques is also predicted by a recent model of cholinergic modulation in the context of a visual attention task (Deco and Thiele, 2011).”

“V1 was identified in all species by using Nissl-stained reference sections, aided by brain atlases and published data (Choudhury, 1978; McConnell and LeVay, 1986; Paxinos and Franklin, 2003; Paxinos et al., 2000; Paxinos and Watson, 2007; White et al., 1999).”

“In the neocortex, ACh is usually released from varicosities that are not apposed to a synaptic specialization (Aoki and Kabak, 1992; Beaulieu and Somogyi, 1991; Umbriaco et al., 1994), a mode of release known as volume transmission (but see Turrini et al., 2001).”

“Three one-in-six series of sections were set aside, one for a Nissl reference set, another for a Gallyas reference set (Gallyas, 1970), and the third for a cytochrome oxidase reference set (Wong-Riley et al., 1998).”

“…is suppressive in the rodent cortex (Gil et al., 1997; Hasselmo and Bower, 1992; Hsieh et al., 2000; Kimura, 2000), as it is in the macaque cortex (Disney et al., 2012), and ACh has been shown to boost thalamic gain in both species (Disney et al., 2007; Gil et al., 1997; Hasselmo and Bower, 1992;…”

“V1 was identified in all species by using Nissl-stained reference sections, aided by brain atlases and published data (Choudhury, 1978; McConnell and LeVay, 1986; Paxinos and Franklin, 2003; Paxinos et al., 2000; Paxinos and Watson, 2007; White et al., 1999).”

“V1 was identified in all species by using Nissl-stained reference sections, aided by brain atlases and published data (Choudhury, 1978; McConnell and LeVay, 1986; Paxinos and Franklin, 2003; Paxinos et al., 2000; Paxinos and Watson, 2007; White et al., 1999).”

“Three one-in-six series of sections were set aside, one for a Nissl reference set, another for a Gallyas reference set (Gallyas, 1970), and the third for a cytochrome oxidase reference set (Wong-Riley et al., 1998).”

“Developing these techniques in non-human primates will be necessary because cell-type-specific expression of neuromodulator receptors can differ radically between rodents and primates (Disney and Reynolds, 2014).”

“Electrical stimulation of these regions diminishes slow cortical synchronization, an effect that is thought to depend on acetylcholine acting upon muscarinic receptors (Metherate et al., 1992; Disney and Reynolds, 2014; but see also Hangya et al., 2015; as well as Raver and Lin, 2015).”

“The neurophysiological role of mACh receptors on neurons remains to be fully elucidated, but evidence indicates that M1-ACh receptors modulate both cortical pyramidal and interneuron activity [102, 103].”

“More than 75 percent of PV-immunoreactive visual cortical neurons in macaques, humans and guinea pigs express M1 mAChRs (Disney and Reynolds, 2014).”

“Cholinergic circuitry differs substantially across brain regions (Disney et al., 2006; Raghanti et al., 2008) and across species (Disney and Reynolds, 2014).”

“, 2008), and the cortical and subcortical expression of nicotinic and muscarinic receptor subtypes (Wada et al., 1989; Marks et al., 1992; Séguéla et al., 1993; Quik et al., 2000; Disney and Reynolds, 2014; Coppola et al., 2016) call for careful interpretation of data across animal models.”

“Further, qualitative data indicate that excitatory neurons in V1 of ferrets and guinea pigs more frequently express the m1 receptor than do excitatory neurons in V1 of macaques or humans (Disney and Reynolds, 2014).”

“For example, several studies report no significant between-area and between-species differences in the size of CR + neurons (Gab-bott & Bacon, 1996a; Gabbott et al., 1997; Kooijmans et al., 2020) or PV + neurons (Disney & Reynolds, 2014; Povysheva et al., 2008).”

“Unfortunately, antibodies directed against m3, m4 and m5 AChRs do not pass controls for use in the macaque monkey (Disney and Reynolds 2014; and A. A. Disney unpubl. data) so these anatomical data are unlikely to become available in the near future.”

“M1R has been found in various cortical neuronal elements including both excitatory neurons (Mrzljak, Levey, & Goldman-Rakic, 1993; Disney, Domakonda, & Aoki, 2006; Yamasaki, Matsui, & Watanabe, 2010) and inhibitory neurons (Disney et al., 2006; Disney & Aoki, 2008; Disney & Reynolds, 2014).”

“It is remains puzzling how an overall facilitation occurs given that nicotinic and muscarinic somatic receptors reside predominantly on inhibitory interneurons (Disney et al., 2006, 2014; Disney and Aoki, 2008; Disney and Reynolds, 2014).”

“For example, muscarinic M1 receptor expression profiles across cell types in V1 show significant species differences, where in human, rhesus macaque, and guinea pig, 74–85% of parvalbumin-expressing GABAergic interneurons also express M1Rs, compared to 27% in rats (Disney and Reynolds, 2014).”

“31), in the pattern of cholinergic innervation of the primary visual cortex (50), and in receptor expression in the visual thalamus (51, 52), the afferent pathway from the thalamus to the primary cortex (33, 37), and within the intrinsic circuitry of V1 (44).”

“…and receptors within V1 (Lysakowski, Wainer, Bruce, & Hersh, 1989; Mechawar, Cozzari, & Descarries, 2000; Wong & Kaas, 2008; Wong & Kaas, 2010; Disney & Reynolds, 2014) and the functional contribution of acetylcholine to receptive field tuning, attentional modulation, and plasticity in V1…”

“In rhesus macaque areas V1 and MT, the majority of parvalbumin-positive interneurons are found to express M1Rs (Disney and Aoki, 2008; Disney and Reynolds, 2014), although it is not clear if this is also the case in PFC. M1R activation leads to Ca2+ mobilization from intracellular stores through…”

“, 2015), and receptor expression patterns (Disney et al., 2006; Disney and Reynolds, 2014) (species differences reviewed by Coppola and Disney, (2018)).”

“…Berry, et al. 2016; Thomsen, Sørensen, and Dencker 2018; Disney and Aoki 2008; Disney, Domakonda, and Aoki 2006; Disney, Alasady, and Reynolds 2014; Disney and Reynolds 2014) and the activity associated with known uncertainty (Monosov, Leopold, and Hikosaka 2015; Voytko et al. 1994; Gill, Sarter,…”

“A key concern with non-stereological approaches is size bias: Abercrombie correction did not change overall proportions, indicating that cell type-specific differences in soma sizes/aspect ratios did not bias our results.”

“However, murine cholinergic aging closely parallels human systems; absolute acetylcholine levels, receptor expression patterns, and acetylcholinesterase isoform distribution differ between species [116,117].”