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PDF of The Marmoset Brain in Stereotaxic Coordinates

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This is the full pdf of the Paxinos et al. 2012 atlas of the marmoset brain. This book has gone out of print, and the copyright reverted to the authors. For more resources related to the marmoset brain, visit www.marmosetbrain.org
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... The distinct gene expression revealed in this study strongly supports the prostriata as an independent anatomical entity (Ding, 2013;Lu et al., 2020) rather than as part of RSg (area 29e) (Blackstad, 1956;Haug, 1976;Slomianka & Geneser, 1991;Vaz Ferreira, 1951) or part of PrS/PoS (Paxinos & Franklin, 2001;Swanson, 2018). The similar topographic relationship of the prostriata with neighboring regions (see Figures 1 and 3) compared to nonhuman primates (Ding et al., 2003;Morecraft et al., 2000; Figure 20) further supports its nature as the equivalent of the primate prostriata (Allman & Kaas, 1971;Ding et al., 2003;Morecraft et al., 2000;Paxinos et al., 2012;Rockland, 2012;Sanides, 1969;Sousa et al., 1991). Similar ...
... Although limited data are available about the chemoarchitecture of nonhuman primates, some previous work showed enriched expression of calbindin-D28k in layers 2-3 of the prostriata in macaque and marmoset monkeys (Ding et al., 2003;Paxinos et al., 2012). Similar findings were reported for the prostriata of the mice and rats (Chen et al., 2021;Lu et al., 2020). ...
... Previous studies in nonhuman primates showed that cingulate cortical area 23 (A23) also adjoins the prostriata (Ding et al., 2003;Paxinos et al., 2012). This indicates that A23 (including A23v; see Figure 20) ...
Article
Retrosplenial area 29e, which was a cortical region described mostly in earlier rodent literature, is often included in the dorsal presubiculum (PrSd) or postsubiculum (PoS) in modern literature and commonly used brain atlases. Recent anatomical and molecular studies have revealed that retrosplenial area 29e belongs to the superficial layers of area prostriata, which in primates is found to be important in fast analysis of quickly moving objects in far peripheral visual field. As in primates, the prostriata in rodents adjoins area 29 (granular retrosplenial area), area 30 (agranular retrosplenial area), medial visual cortex, PrSd/PoS, parasubiculum (PaS), and postrhinal cortex (PoR). The present study aims to reveal the chemoarchitecture of the prostriata versus PrSd/PoS or PaS by means of a systematic survey of gene expression patterns in adult and developing mouse brains. First, we find many genes that display differential expression across the prostriata, PrSd/PoS, and PaS and that show obvious laminar expression patterns. Second, we reveal subsets of genes that selectively express in the dorsal or ventral parts of the prostriata, suggesting the existence of at least two subdivisions. Third, we detect some genes that shows differential expression in the prostriata of postnatal mouse brains from adjoining regions, thus enabling identification of the developing area prostriata. Fourth, gene expression difference of the prostriata from the medial primary visual cortex and PoR is also observed. Finally, molecular and connectional features of the prostriata in rodents and nonhuman primates are discussed and compared.
... Spatial coordinates are a fundamental framework for understanding the brain through mapping cells, architectures and functions. Stereotactic devices are widely used in animal neuroscience and offer a coordinate to map and target specific brain regions (Hardman and Ashwell, 2012;Palazzi and Bordier, 2009;Paxinos et al., 2012;Stephan et al., 1980;Yuasa et al., 2010). Atlases in stereotactic coordinates are commonly based on a single subject's ex-vivo brain histology data (Bowden and Martin, 2000;Hardman and Ashwell, 2012;Paxinos and Franklin, 2019;Paxinos and Watson, 2017;Saleem and Logothetis, 2006). ...
... We discuss registration accuracy, anatomical variability, templates and atlas, bias between stereotactic and AC-PC coordinates, and neuroimage-based targeting in marmoset. Rodents (Paxinos and Franklin, 2019;Paxinos and Watson, 2017), Marmoset (Hardman and Ashwell, 2012;Palazzi and Bordier, 2009;Paxinos et al., 2012;Stephan et al., 1980;Yuasa et al., 2010;Woodward et al., 2018), Macaque (Horsley and Clarke, 1908;Paxinos et al., 1999;Saleem and Logothetis, 2006;Hartig et al., 2021; Histology Ex-vivo MRI ...
... We also investigated cortical surface landmark intersubject variability. Specifically, we focused on the intraparietal sulcus (IPS) because it is a recognizable landmark in marmosets (Fig. 7b) Paxinos et al., 2012). We quantitatively defined the presence of the IPS based on the values of the FreeSurfer 'sulc' measure in each subject's 32k mesh, and identified the local minimum in a region of interest (IPS ROI), which comprises four intraparietal areas (anterior intraparietal [AIP], medial intraparietal [MIP], lateral intraparietal [LIP], and ventral intraparietal [VIP] areas). ...
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Localising accurate brain regions needs careful evaluation in each experimental species due to their individual variability. However, the function and connectivity of brain areas is commonly studied using a single-subject cranial landmark-based stereotactic atlas in animal neuroscience. Here, we address this issue in a small primate, the common marmoset, which is increasingly widely used in systems neuroscience. We developed a non-invasive multi-modal neuroimaging-based targeting pipeline, which accounts for intersubject anatomical variability in cranial and cortical landmarks in marmosets. This methodology allowed creation of multi-modal templates (MarmosetRIKEN20) including head CT and brain MR images, embedded in coordinate systems of anterior and posterior commissures (AC-PC) and CIFTI grayordinates. We found that the horizontal plane of the stereotactic coordinate was significantly rotated in pitch relative to the AC-PC coordinate system (10 degrees, frontal downwards), and had a significant bias and uncertainty due to positioning procedures. We also found that many common cranial and brain landmarks (e.g., bregma, intraparietal sulcus) vary in location across subjects and are substantial relative to average marmoset cortical area dimensions. Combining the neuroimaging-based targeting pipeline with robot-guided surgery enabled proof-of-concept targeting of deep brain structures with an accuracy of 0.2 mm. Altogether, our findings demonstrate substantial intersubject variability in marmoset brain and cranial landmarks, implying that subject-specific neuroimaging-based localization is needed for precision targeting in marmosets. The population-based templates and atlases in grayordinates, created for the first time in marmoset monkeys, should help bridging between macroscale and microscale analyses. Highlights Achieved sub-millimeter localization accuracy of subject-wise brain region Propose a dedicated non-invasive multi-modal subject-specific registration pipeline Construct brain coordinate system in AC-PC and grayordinate spaces Establish multi-modal MRI and CT brain and cortical templates, MarmosetRIKEN20 Quantify intersubject variabilities in marmoset brain Significant bias and uncertainty exist in marmoset stereotactic positioning
... Stereotaxic procedures in the marmoset, including electrophysiological recordings (Debnath et al., 2018;Pomberger and Hage, 2019), lesion, and tracer mapping studies (Liebetanz et al., 2002;Abe et al., 2017) have been guided by two-dimensional (2D) brain atlases. However, the majority of atlases have collected data from a restricted number of animals (Stephan et al., 1980;Tokuno et al., 2009;Paxinos et al., 2012) or a single sex (Stephan et al., 1980), which fail to account for the variable skull and brain size between animals. Whilst recent atlases of the marmoset brain have employed relatively larger sample sizes (N = 5-20) to address individual variability (Liu et al., 2018;Risser et al., 2019;Majka et al., 2021), some templates only collected data from a single subject (Liu et al., 2018;Risser et al., 2019), a common practice of stereotaxic atlases. ...
... Briefly, a 3D reconstructed skull surface of the marmoset, derived from the MRI or CT, is used along with a laser light source to identify homologous points on the actual skull of the animal in surgery within a common coordinate space (Orringer et al., 2012). By using 3D coordinates that are unique to each animal, precision in localising targets is enhanced, which is crucial in procedures that use marmosets, whereas conventional stereotaxic atlases fail to address inter-individual variation between animals (Tokuno et al., 2009;Paxinos et al., 2012). ...
... Renewed interest in marmosets for neuroscience research, including large-scale initiatives to map their brain (Okano et al., 2016;Liu et al., 2020), depends on accurate localisation of brain structures. While these endeavours have largely relied on 2D stereotaxic atlases of the marmoset brain (Stephan et al., 1980;Tokuno et al., 2009;Paxinos et al., 2012), they fail to account for the variability in brain and skull size amongst animals due to a limited sample size (Franc¸ois et al., 1996;Deogaonkar et al., 2005;Miocinovic et al., 2007). These issues have led to the advent of averaged templates of the marmoset brain (Liu et al., 2018;Risser et al., 2019;Majka et al., 2021), which incorporate individual variability and consequently, provide a more accurate localisation of brain structures. ...
Article
Full-text available
The common marmoset has emerged as a popular model in neuroscience research, in part due to its reproductive efficiency, genetic and neuroanatomical similarities to humans and the successful generation of transgenic lines. Stereotaxic procedures in marmosets are guided by 2D stereotaxic atlases, which are constructed with a limited number of animals and fail to account for inter-individual variability in skull and brain size. Here, we developed a frameless imaging-guided stereotaxic system that improves upon traditional approaches by using subject-specific registration of computed tomography (CT), magnetic resonance imaging (MRI) and positron emission tomography (PET) data to identify a surgical target, namely the putamen, in two marmosets. The skull surface was laser-scanned with to create a point cloud that was registered to the 3D reconstruction of the skull from CT. Reconstruction of the skull, as well as of the brain from MR images, was crucial for surgical planning. Localisation and injection into the putamen was done using a 6-axis robotic arm controlled by a surgical navigation software (BrainsightTM). Integration of subject-specific registration and frameless stereotaxic navigation allowed target localisation specific to each animal. Injection of alpha-synuclein fibrils into the putamen triggered progressive neurodegeneration of the nigro-striatal system, a key feature of Parkinson’s disease. Four months post-surgery, a PET scan found evidence of nigro-striatal denervation, supporting accurate targeting of the putamen during co-registration and subsequent surgery. Our results suggest that this approach, coupled with frameless stereotaxic neuronavigation, is accurate in localising surgical targets and can be used to assess endpoints for longitudinal studies.
... Stereotaxic injections were performed using a stereotaxic frame (Kopf Instruments) under general anesthesia with xylazine/ketamine (10 mg kg −1 and 150 mg kg −1 , respectively). Anatomical coordinates and maps were adjusted from Watson and Paxinos 74 . The injection rate was set at 100 nl min −1 . ...
... Adult male mice (6-12 weeks) were anesthetized with chloral hydrate (8%), 400 mg/kg i.p. supplemented as required to maintain optimal anesthesia throughout the experiment and positioned in a stereotaxic frame. A hole was drilled in the skull above midbrain dopaminergic nuclei (coordinates: 3 ± 0.3 mm posterior to bregma, 0.5 ± 0.1 mm [VTA] lateral to the midline) 74 . Recording electrodes were pulled from borosilicate glass capillaries (with outer and inner diameters of 1.50 and 1.17 mm, respectively) with a Narishige electrode puller. ...
Article
Full-text available
Enduring behavioral changes upon stress exposure involve changes in gene expression sustained by epigenetic modifications in brain circuits, including the mesocorticolimbic pathway. Brahma (BRM) and Brahma Related Gene 1 (BRG1) are ATPase subunits of the SWI/SNF complexes involved in chromatin remodeling, a process essential to enduring plastic changes in gene expression. Here, we show that in mice, social defeat induces changes in BRG1 nuclear distribution. The inactivation of the Brg1/Smarca4 gene within dopamine-innervated regions or the constitutive inactivation of the Brm/Smarca2 gene leads to resilience to repeated social defeat and decreases the behavioral responses to cocaine without impacting midbrain dopamine neurons activity. Within striatal medium spiny neurons, Brg1 gene inactivation reduces the expression of stress- and cocaine-induced immediate early genes, increases levels of heterochromatin and at a global scale decreases chromatin accessibility. Altogether these data demonstrate the pivotal function of SWI/SNF complexes in behavioral and transcriptional adaptations to salient environmental challenges. Repeated exposure to social stressors in rodents results in behavioural changes. Here the authors show that behavioural adaptations to stress are associated with nuclear organization changes through SWI/SNF chromatin remodeler in specific neuronal populations of the mesolimbic system.
... One approach to addressing these discrepancies and to bridge this apparent gap between rodent and human studies is to determine the contribution of these regions of vmPFC in a non-human primate in which the overall structural organization of vmPFC is far similar to that of humans than that of rodents (Ongür & Price, 2000;Paxinos et al., 2011). Already the use of anatomical tracing (Chiba et al., 2001;Freedman et al., 2000;Joyce & Barbas, 2018;Ongür & Price, 2000) and electrophysiological recordings (Amemori & Graybiel, 2012;Monosov & Hikosaka, 2012) in macaques has begun to highlight the heterogeneity in connections and functional representations within the vmPFC. ...
Article
Neuroimaging studies implicate the ventromedial prefrontal cortex (vmPFC) in a wide range of emotional and cognitive functions, and changes in activity within vmPFC have been linked to the aetiology and successful treatment of depression. However, this is a large, structurally heterogeneous region and the extent to which this structural heterogeneity reflects functional heterogeneity remains unclear. Causal studies in animals should help address this question but attempts to map findings from vmPFC studies in rodents onto human imaging studies highlight cross-species discrepancies between structural homology and functional analogy. Bridging this gap, recent studies in marmosets - a species of new world monkey in which the overall organization of vmPFC is more like humans than that of rodents - have revealed that over-activation of the caudal subcallosal region of vmPFC, area 25, but not neighbouring area 32, heightens reactivity to negatively valenced stimuli whilst blunting responsivity to positively valenced stimuli. These co-occurring states resemble those seen in depressed patients, which are associated with increased activity in caudal subcallosal regions. In contrast, only reward blunting but not heightening of threat reactivity is seen following over-activation of the structurally homologous region in rodents. To further advance understanding of the role of vmPFC in the aetiology and treatment of depression, future work should focus on the behaviourally specific networks by which vmPFC regions have their effects, together with characterization of cross-species similarities and differences in function.
... The endopiriform nuclear complex of the tree pangolin could be parcellated into three nuclei-dorsal, intermediate, and ventral. This nuclear organization appears to conform to that reported in the brains of laboratory rodents (e.g., Paxinos & Watson, 2007;) and primates (e.g., Paxinos et al., 2000;Paxinos et al., 2012), and may be indicative of the nuclear organization of the endopiriform nuclear complex across mammals generally (Smith et al., 2018). In this sense, the functional aspects of the endopiriform nuclear complex in the tree pangolin likely correlate with that observed in other mammals, especially given the organization of the olfactory system in the tree pangolin (Imam et al., 2018a). ...
Article
A cyto‐, myelo‐, and chemoarchitectonic analysis of the pallial telencephalon of the tree pangolin is provided. As certain portions of the pallial telencephalon have been described previously (olfactory pallium, hippocampal formation, and amygdaloid complex), we focus on the claustrum and endopiriform nuclear complex, the white matter and white matter interstitial cells, and the areal organization of the cerebral cortex. Our analysis indicates that the organization of the pallial telencephalon of the tree pangolin is similar to that observed in many other mammals, and specifically quite similar to the closely related carnivores. The claustrum of the tree pangolin exhibits a combination of insular and laminar architecture, while the endopiriform nuclear complex contains three nuclei, both reminiscent of observations made in other mammals. The population of white matter interstitial cells resembles that observed in other mammals, while a distinct laminated organization of the intracortical white matter was revealed with parvalbumin immunostaining. The cerebral cortex of the tree pangolin presented with indistinct laminar boundaries as well as pyramidalization of the neurons in both layers 2 and 4. All cortical regions typically found in mammals were present, with the cortical areas within these regions often corresponding to what has been reported in carnivores. Given the similarity of the organization of the pallial telencephalon of the tree pangolin to that observed in other mammals, especially carnivores, it would be reasonable to assume that the neural processing afforded the tree pangolin by these structures does not differ dramatically to that of other mammals. Lateral view of the brain of the tree pangolin with the various cortical areas (each area being a different color) determined through cyto‐, myelo‐, and chemoarchitectural analysis. The areal organization of the tree pangolin cerebral cortex follows that observed in the closely related carnivores.
... Cortical slices (350 μm thick) were prepared from 28-32 days-old male wild type and mutant Lis1/sLis1-GAD67-GFP mice, using standard methods used in our laboratory (Rovira and Geijo-Barrientos, 2016;Sempere-Ferrandez et al., 2018). The slices were oriented coronally and included the primary motor cortex (at 1.30 mm anterior to Bregma according to the mouse brain atlas by Paxinos and Watson, 2001). Animals were sacrificed by cervical dislocation and coronal slices were cut with a Vibratome (Leica VT1000) in ice-cold low calcium/high magnesium cutting solution (composition: 124 mM NaCl, 2.5 mM KCl, 1.25 mM PO 4 H 2 Na, 2.5 mM MgCl 2 , 0.5 mM CaCl 2 , 26 mM NaCO 3 H and 10 mM glucose; pH 7.4 when saturated with 95% O 2 and 5% CO 2 ). ...
Article
Full-text available
LIS1 (PAFAH1B1) plays a major role in the developing cerebral cortex, and haploinsufficient mutations cause human lissencephaly type 1. We have studied morphological and functional properties of the cerebral cortex of mutant mice harboring a deletion in the first exon of the mouse Lis1 (Pafah1b1) gene, which encodes for the LisH domain. The Lis1/sLis1 animals had an overall unaltered cortical structure but showed an abnormal distribution of cortical GABAergic interneurons (those expressing calbindin, calretinin, or parvalbumin), which mainly accumulated in the deep neocortical layers. Interestingly, the study of the oscillatory activity revealed an apparent inability of the cortical circuits to produce correct activity patterns. Moreover, the fast spiking (FS) inhibitory GABAergic interneurons exhibited several abnormalities regarding the size of the action potentials, the threshold for spike firing, the time course of the action potential after-hyperpolarization (AHP), the firing frequency, and the frequency and peak amplitude of spontaneous excitatory postsynaptic currents (sEPSC's). These morphological and functional alterations in the cortical inhibitory system characterize the Lis1/sLis1 mouse as a model of mild lissencephaly, showing a phenotype less drastic than the typical phenotype attributed to classical lissencephaly. Therefore, the results described in the present manuscript corroborate the idea that mutations in some regions of the Lis1 gene can produce phenotypes more similar to those typically described in schizophrenic and autistic patients and animal models.
... Recordings were controlled and analyzed offline using Axograph (Axograph). The locations of all recorded cells were mapped according to the Mouse Brain Atlas (Paxinos and Watson, 2019). The liquid junction potential (;9 mV) was not compensated for. ...
Article
Decisions to act while pursuing goals in the presence of danger must be made quickly but safely. Premature decisions risk injury or death whereas postponing decisions risk goal loss. Here we show how mice resolve these competing demands. Using microstructural behavioral analyses, we identified the spatiotemporal dynamics of approach-avoidance decisions under motivational conflict in male mice. Then we used cognitive modelling to show that these dynamics reflect the speeded decision-making mechanisms used by humans and non-human primates, with mice trading off decision speed for safety of choice when danger loomed. Using calcium imaging in paraventricular thalamus and optogenetic inhibition of the prelimbic cortex to paraventricular thalamus pathway, we show that this speed-safety trade off occurs because increases in paraventricular thalamus activity increase decision caution, thereby increasing approach-avoid decision times in the presence of danger. Our findings demonstrate that a discrete brain circuit involving the paraventricular thalamus and its prefrontal input adjusts decision caution during motivational conflict, trading off decision speed for decision safety when danger is close. We identify the corticothalamic pathway as central to cognitive control during decision-making under conflict.Significance Statement:Foraging animals balance the need to seek food and energy against the conflicting needs to avoid injury and predation. This competition is fundamental to survival, but rarely has a stable, correct solution. Here we show that approach - avoid decisions under motivational conflict involves strategic adjustments in decision caution controlled via a top-down corticothalamic pathway from the prelimbic cortex to the paraventricular thalamus. We identify a novel corticothalamic mechanism for cognitive control that is applicable across a range of motivated behaviours and mark paraventricular thalamus and its prefrontal cortical input as targets to remediate the deficits in decision caution characteristic of unsafe and impulsive choices.
... To help annotate the regions where the electrodes were attached to the brain surface, the cortical annotation of the marmoset MR imaging atlas 58 was transformed onto the subject space by using a free-form deformation named Symmetric Normalization, implemented in the ANTs toolbox 59 . We determined the putative cortical areas of the electrodes based on visual inspection of the MR images compared to the standard atlas 60 and digital annotation based on spatial deformation on the subject brain. ...
Article
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Numerous studies have shown that the visual system consists of functionally distinct ventral and dorsal streams; however, its exact spatial-temporal dynamics during natural visual behavior remain to be investigated. Here, we report cerebral neural dynamics during active visual exploration recorded by an electrocorticographic array covering the entire lateral surface of the marmoset cortex. We found that the dorsal stream was activated before the primary visual cortex with saccades and followed by the alteration of suppression and activation signals along the ventral stream. Similarly, the signal that propagated from the dorsal to ventral visual areas was accompanied by a travelling wave of low frequency oscillations. Such signal dynamics occurred at an average of 220 ms after saccades, which corresponded to the timing when whole-brain activation returned to background levels. We also demonstrated that saccades could occur at any point of signal flow, indicating the parallel computation of motor commands. Overall, this study reveals the neural dynamics of active vision, which are efficiently linked to the natural rhythms of visual exploration.
Article
Social-cognitive processes facilitate the use of environmental cues to understand others, and to be understood by others. Animal models provide vital insights into the neural underpinning of social behaviours. To understand social cognition at even deeper behavioural, cognitive, neural, and molecular levels, we need to develop more representative study models, which allow testing of novel hypotheses using human-relevant cognitive tasks. Due to their cooperative breeding system and relatively small size, common marmosets (Callithrix jacchus) offer a promising translational model for such endeavours. In addition to having social behavioural patterns and group dynamics analogous to those of humans, marmosets have cortical brain areas relevant for the mechanistic analysis of human social cognition, albeit in simplified form. Thus, they are likely suitable animal models for deciphering the physiological processes, connectivity and molecular mechanisms supporting advanced cognitive functions. Here, we review findings emerging from marmoset social and behavioural studies, which have already provided significant insights into executive, motivational, social, and emotional dysfunction associated with neurological and psychiatric disorders.
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