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Comparative density of CCK- and PV-GABA cells within the cortex and hippocampus.

Whissell PD, Cajanding JD, Fogel N, Kim JC - Front Neuroanat (2015)

Bottom Line: However, the relationship and balance between CCK- and PV-GABA neurons in the inhibitory networks of the brain is currently unclear as the distribution of these cells has never been compared on a large scale.The reverse trend was observed for PV-GABA cells.The intersectional genetic labeling approach employed in the current study expands upon the ability to study molecularly defined subsets of GABAergic neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Toronto, Toronto ON, Canada.

ABSTRACT
Cholecystokinin (CCK)- and parvalbumin (PV)-expressing neurons constitute the two major populations of perisomatic GABAergic neurons in the cortex and the hippocampus. As CCK- and PV-GABA neurons differ in an array of morphological, biochemical and electrophysiological features, it has been proposed that they form distinct inhibitory ensembles which differentially contribute to network oscillations and behavior. However, the relationship and balance between CCK- and PV-GABA neurons in the inhibitory networks of the brain is currently unclear as the distribution of these cells has never been compared on a large scale. Here, we systemically investigated the distribution of CCK- and PV-GABA cells across a wide number of discrete forebrain regions using an intersectional genetic approach. Our analysis revealed several novel trends in the distribution of these cells. While PV-GABA cells were more abundant overall, CCK-GABA cells outnumbered PV-GABA cells in several subregions of the hippocampus, medial prefrontal cortex and ventrolateral temporal cortex. Interestingly, CCK-GABA cells were relatively more abundant in secondary/association areas of the cortex (V2, S2, M2, and AudD/AudV) than they were in corresponding primary areas (V1, S1, M1, and Aud1). The reverse trend was observed for PV-GABA cells. Our findings suggest that the balance between CCK- and PV-GABA cells in a given cortical region is related to the type of processing that area performs; inhibitory networks in the secondary cortex tend to favor the inclusion of CCK-GABA cells more than networks in the primary cortex. The intersectional genetic labeling approach employed in the current study expands upon the ability to study molecularly defined subsets of GABAergic neurons. This technique can be applied to the investigation of neuropathologies which involve disruptions to the GABAergic system, including schizophrenia, stress, maternal immune activation and autism.

No MeSH data available.


Related in: MedlinePlus

CCK-GABA cells are most numerous within the medial prefrontal cortex. (Top) Sections of the prefrontal cortex in CCK- and PV-Frepe mice. (Bottom) Percentage contribution of CCK- and PV-GABA cells to the total GABA neuron population by subregion of the frontal cortex. In the DP and IL regions, CCK-GABA cells were more abundant than PV-GABA cells. CCK-GABA cells also tended to be more abundant in the PL region. PV-GABA cells were more abundant in M1 region and tended to be more abundant in the M2 region. Abbreviations: Cg, cingulate cortex, DP, dorsal peduncular region, IL, infralimbic cortex, M1, primary motor cortex, M2, secondary motor cortex, PL, prelimbic cortex. Significance at the p < 0.05 level is denoted with an asterisk. Scale bar = 500 μM.
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Figure 3: CCK-GABA cells are most numerous within the medial prefrontal cortex. (Top) Sections of the prefrontal cortex in CCK- and PV-Frepe mice. (Bottom) Percentage contribution of CCK- and PV-GABA cells to the total GABA neuron population by subregion of the frontal cortex. In the DP and IL regions, CCK-GABA cells were more abundant than PV-GABA cells. CCK-GABA cells also tended to be more abundant in the PL region. PV-GABA cells were more abundant in M1 region and tended to be more abundant in the M2 region. Abbreviations: Cg, cingulate cortex, DP, dorsal peduncular region, IL, infralimbic cortex, M1, primary motor cortex, M2, secondary motor cortex, PL, prelimbic cortex. Significance at the p < 0.05 level is denoted with an asterisk. Scale bar = 500 μM.

Mentions: Within the frontal cortex, GFP-labeled cells were counted in the cingulate cortex (Cg), dorsal peduncular region (DP), infralimbic (IL) cortex, primary motor cortex (M1), secondary motor cortex (M2) and prelimbic (PL) cortex (Figure 3, Table 1). These particular subregions of the frontal cortex are relatively easy to distinguish, contain elaborate networks of CCK- and PV-GABA neurons, and are implicated in the pathogenesis of neurodegenerative and neuropsychiatric diseases (Bachus et al., 1997; Penschuck et al., 2006; Abdul-Monim et al., 2007; Braun et al., 2007; Falco et al., 2014; Uchida et al., 2014; Wischhof et al., 2015). Two-way ANOVA detected a significant interaction of genotype × brain region on the percentage of GFP-labeled cells [F(5,48) = 11.27, p < 0.001]. Within the IL and DP regions of the frontal cortex, CCK-GABA cells were more numerous than PV-GABA cells (ps < 0.05; Figure 3). In the PL, CCK-GABA cells also tended to be more numerous, though the difference was not significant. In contrast to the relative abundance of CCK-GABA cells in medial prefrontal cortex subregions (IL/PL/Cg), PV-GABA cells were significantly more abundant in the M1 subregion (ps < 0.05, Figure 3) and tended to be more abundant in M2 subregion. Collectively, PV-GABA cells constituted ∼40% of all GABAergic cells in M1 and M2, as shown previously (Conde et al., 1994; Tamamaki et al., 2003; Uchida et al., 2014). There were no differences in the percentages of CCK- and PV-GABA cells in the Cg (p > 0.05). In summary, these data suggest that CCK-GABA cells comprise a larger proportion of the GABAergic population in the medial prefrontal cortex than in the adjacent motor cortex.


Comparative density of CCK- and PV-GABA cells within the cortex and hippocampus.

Whissell PD, Cajanding JD, Fogel N, Kim JC - Front Neuroanat (2015)

CCK-GABA cells are most numerous within the medial prefrontal cortex. (Top) Sections of the prefrontal cortex in CCK- and PV-Frepe mice. (Bottom) Percentage contribution of CCK- and PV-GABA cells to the total GABA neuron population by subregion of the frontal cortex. In the DP and IL regions, CCK-GABA cells were more abundant than PV-GABA cells. CCK-GABA cells also tended to be more abundant in the PL region. PV-GABA cells were more abundant in M1 region and tended to be more abundant in the M2 region. Abbreviations: Cg, cingulate cortex, DP, dorsal peduncular region, IL, infralimbic cortex, M1, primary motor cortex, M2, secondary motor cortex, PL, prelimbic cortex. Significance at the p < 0.05 level is denoted with an asterisk. Scale bar = 500 μM.
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Related In: Results  -  Collection

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Figure 3: CCK-GABA cells are most numerous within the medial prefrontal cortex. (Top) Sections of the prefrontal cortex in CCK- and PV-Frepe mice. (Bottom) Percentage contribution of CCK- and PV-GABA cells to the total GABA neuron population by subregion of the frontal cortex. In the DP and IL regions, CCK-GABA cells were more abundant than PV-GABA cells. CCK-GABA cells also tended to be more abundant in the PL region. PV-GABA cells were more abundant in M1 region and tended to be more abundant in the M2 region. Abbreviations: Cg, cingulate cortex, DP, dorsal peduncular region, IL, infralimbic cortex, M1, primary motor cortex, M2, secondary motor cortex, PL, prelimbic cortex. Significance at the p < 0.05 level is denoted with an asterisk. Scale bar = 500 μM.
Mentions: Within the frontal cortex, GFP-labeled cells were counted in the cingulate cortex (Cg), dorsal peduncular region (DP), infralimbic (IL) cortex, primary motor cortex (M1), secondary motor cortex (M2) and prelimbic (PL) cortex (Figure 3, Table 1). These particular subregions of the frontal cortex are relatively easy to distinguish, contain elaborate networks of CCK- and PV-GABA neurons, and are implicated in the pathogenesis of neurodegenerative and neuropsychiatric diseases (Bachus et al., 1997; Penschuck et al., 2006; Abdul-Monim et al., 2007; Braun et al., 2007; Falco et al., 2014; Uchida et al., 2014; Wischhof et al., 2015). Two-way ANOVA detected a significant interaction of genotype × brain region on the percentage of GFP-labeled cells [F(5,48) = 11.27, p < 0.001]. Within the IL and DP regions of the frontal cortex, CCK-GABA cells were more numerous than PV-GABA cells (ps < 0.05; Figure 3). In the PL, CCK-GABA cells also tended to be more numerous, though the difference was not significant. In contrast to the relative abundance of CCK-GABA cells in medial prefrontal cortex subregions (IL/PL/Cg), PV-GABA cells were significantly more abundant in the M1 subregion (ps < 0.05, Figure 3) and tended to be more abundant in M2 subregion. Collectively, PV-GABA cells constituted ∼40% of all GABAergic cells in M1 and M2, as shown previously (Conde et al., 1994; Tamamaki et al., 2003; Uchida et al., 2014). There were no differences in the percentages of CCK- and PV-GABA cells in the Cg (p > 0.05). In summary, these data suggest that CCK-GABA cells comprise a larger proportion of the GABAergic population in the medial prefrontal cortex than in the adjacent motor cortex.

Bottom Line: However, the relationship and balance between CCK- and PV-GABA neurons in the inhibitory networks of the brain is currently unclear as the distribution of these cells has never been compared on a large scale.The reverse trend was observed for PV-GABA cells.The intersectional genetic labeling approach employed in the current study expands upon the ability to study molecularly defined subsets of GABAergic neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Toronto, Toronto ON, Canada.

ABSTRACT
Cholecystokinin (CCK)- and parvalbumin (PV)-expressing neurons constitute the two major populations of perisomatic GABAergic neurons in the cortex and the hippocampus. As CCK- and PV-GABA neurons differ in an array of morphological, biochemical and electrophysiological features, it has been proposed that they form distinct inhibitory ensembles which differentially contribute to network oscillations and behavior. However, the relationship and balance between CCK- and PV-GABA neurons in the inhibitory networks of the brain is currently unclear as the distribution of these cells has never been compared on a large scale. Here, we systemically investigated the distribution of CCK- and PV-GABA cells across a wide number of discrete forebrain regions using an intersectional genetic approach. Our analysis revealed several novel trends in the distribution of these cells. While PV-GABA cells were more abundant overall, CCK-GABA cells outnumbered PV-GABA cells in several subregions of the hippocampus, medial prefrontal cortex and ventrolateral temporal cortex. Interestingly, CCK-GABA cells were relatively more abundant in secondary/association areas of the cortex (V2, S2, M2, and AudD/AudV) than they were in corresponding primary areas (V1, S1, M1, and Aud1). The reverse trend was observed for PV-GABA cells. Our findings suggest that the balance between CCK- and PV-GABA cells in a given cortical region is related to the type of processing that area performs; inhibitory networks in the secondary cortex tend to favor the inclusion of CCK-GABA cells more than networks in the primary cortex. The intersectional genetic labeling approach employed in the current study expands upon the ability to study molecularly defined subsets of GABAergic neurons. This technique can be applied to the investigation of neuropathologies which involve disruptions to the GABAergic system, including schizophrenia, stress, maternal immune activation and autism.

No MeSH data available.


Related in: MedlinePlus