Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat

Brückner, Gert; Seeger, Gudrun; Brauer, K; Härtig, Wolfgang; Kacza, Johannes; Bigl, Volker

doi:10.1016/s0006-8993(09)90012-9

Cited by 123 publications

(72 citation statements)

References 72 publications

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“…1E), similar to the mammalian A1 (43,44). Individual layers of the chick CM and Field L, particularly the sublayers of the CM and L1, are readily apparent in sections stained with parvalbumin immunoreactivity.…”

Section: Resultsmentioning

confidence: 71%

Laminar and columnar auditory cortex in avian brain

Wang

Brzozowska-Prechtl

Karten

2010

Proc. Natl. Acad. Sci. U.S.A.

225

223

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The mammalian neocortex mediates complex cognitive behaviors, such as sensory perception, decision making, and language. The evolutionary history of the cortex, and the cells and circuitry underlying similar capabilities in nonmammals, are poorly understood, however. Two distinct features of the mammalian neocortex are lamination and radially arrayed columns that form functional modules, characterized by defined neuronal types and unique intrinsic connections. The seeming inability to identify these characteristic features in nonmammalian forebrains with earlier methods has often led to the assumption of uniqueness of neocortical cells and circuits in mammals. Using contemporary methods, we demonstrate the existence of comparable columnar functional modules in laminated auditory telencephalon of an avian species (Gallus gallus). A highly sensitive tracer was placed into individual layers of the telencephalon within the cortical region that is similar to mammalian auditory cortex. Distribution of anterograde and retrograde transportable markers revealed extensive interconnections across layers and between neurons within narrow radial columns perpendicular to the laminae. This columnar organization was further confirmed by visualization of radially oriented axonal collaterals of individual intracellularly filled neurons. Common cell types in birds and mammals that provide the cellular substrate of columnar functional modules were identified. These findings indicate that laminar and columnar properties of the neocortex are not unique to mammals and may have evolved from cells and circuits found in more ancient vertebrates. Specific functional pathways in the brain can be analyzed in regard to their common phylogenetic origins, which introduces a previously underutilized level of analysis to components involved in higher cognitive functions. neocortex evolution | columnar organization | primary auditory cortex | intrinsic circuitry | granule cell T he origins and evolution of the forebrain and the mammalian neocortex,* where complex cognitive functions are centered, have long been of broad interest to scientists and nonscientists alike. For more than 100 y, the neocortex was considered an independently evolved structure unique to mammals. The nonmammalian telencephalon was frequently compared with the mammalian basal ganglia, which was thought to be involved in stereotypical instinctive behaviors (1). A revolutionary revision in our concept of the nature of vertebrate brain organization was recently accepted in the revised nomenclature of the avian brain (2, 3). The avian Wulst and dorsal ventricular ridge, two prominent components of the telencephalon, are recognized as being homologous to pallial components of mammalian brains, which is consistent with the idea that avian telencephalon includes a large cortical component ( Fig. 1 A-C) (4-6). However, this postulated homology addresses only the most general aspects of the evolutionary relationship of the avian brain to the mammal brain, that is, in indicating that ...

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Section: Resultsmentioning

confidence: 71%

Laminar and columnar auditory cortex in avian brain

Wang

Brzozowska-Prechtl

Karten

2010

Proc. Natl. Acad. Sci. U.S.A.

225

223

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“…Prior studies have shown that the sensory and motor cortices have high levels of PNN whereas higher association areas have relatively less PNN expression (Hockfield and McKay 1983;Hendry et al 1988;McGuire et al 1989;Bruckner et al 1994Bruckner et al , 1999Bruckner et al , 2008Hausen et al 1996). As it is thought that PNNs stabilize synaptic connectivity, it has been suggested that areas with high PNN levels may be less plastic (Gati et al 2010;Bartus et al 2012;McRae and Porter 2012).…”

Section: Discussionmentioning

confidence: 99%

“…The backbone of the PNN is hyaluronic acid (HA; also known as a hyaluronan or hyaluronate) to which chondroitin sulfate proteoglycans (CSPGs) are covalently linked. It has been reported that the primary sensory and motor areas contain considerably more PNN than secondary or higher order association areas in the adult brain (Hockfield and McKay 1983;Hendry et al 1988;McGuire et al 1989;Bruckner et al 1994Bruckner et al , 1999Bruckner et al , 2008Hausen et al 1996). As secondary and association regions are thought to be more plastic than primary sensory and motor areas, it has been suggested that the PNN may also play a role in regulating synaptic plasticity in the adult brain.…”

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confidence: 99%

Disruption of the perineuronal net in the hippocampus or medial prefrontal cortex impairs fear conditioning

et al. 2013

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The perineuronal net (PNN) surrounds neurons in the central nervous system and is thought to regulate developmental plasticity. A few studies have shown an involvement of the PNN in hippocampal plasticity and memory storage in adult animals. In addition to the hippocampus, plasticity in the medial prefrontal cortex (mPFC) has been demonstrated to be critical for the storage of long-term memory, particularly memories for temporally separated events. In the present study, we examined the role of PNN in the acquisition and retention of memories for trace (in which the conditioned and unconditioned stimuli are temporally separated) and delayed (in which the conditioned and unconditioned stimuli overlap) fear conditioning in both the hippocampus and the mPFC. Consistent with a role for the hippocampus in memory storage in both delayed and trace fear conditioning, removal of hippocampal PNN disrupted contextual and trace fear memory. Disruption of the PNN in the mPFC impaired long-term trace and conditioned stimulus (CS)-elicited fear memory in the trace fear conditioning task. Interestingly, CS-elicited fear memory was also impaired when a delayed fear conditioning paradigm was used. These findings further support a role for the PNN in neural plasticity and implicate PNN-regulated plasticity in neocortical memory storage.

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“…The ECM within ACx consists of compact PNNs enwrapping mainly parvalbumine-positive cells and the more diffuse ubiquitious ECM, both built up by proteoglycans like the chondroitin sulfate proteoglycans (CSPGs) and glycoproteins organized around the ECM's backbone the glycosaminoglycan hyaluronic acid (2,17). To specifically assess the depletion of the ECM within ACx, we injected the glycosidase HYase and 0.9% saline in opposing hemispheres of naïve animals at the age of ≥3 mo (n = 11), a time point when the mature ECM is formed (Fig.…”

Section: Local Removal Of the Ecm In Adult Acx And Its Temporal Reappmentioning

confidence: 99%

“…In the present study, we aimed at evaluating the potential role of experimental ECM removal within the auditory cortex (ACx) of Mongolian gerbils, which has been found to be particularly rich in ECM (17), during a cognitively demanding auditory go/no go shuttle-box task. We selected discrimination and reversal learning of frequency-modulated (FM) tones as a cognitive task, which necessarily requires ACx plasticity (18,19).…”

mentioning

confidence: 99%

Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex

Happel

Niekisch²,

Rivera³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

142

118

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During brain maturation, the occurrence of the extracellular matrix (ECM) terminates juvenile plasticity by mediating structural stability. Interestingly, enzymatic removal of the ECM restores juvenile forms of plasticity, as for instance demonstrated by topographical reconnectivity in sensory pathways. However, to which degree the mature ECM is a compromise between stability and flexibility in the adult brain impacting synaptic plasticity as a fundamental basis for learning, lifelong memory formation, and higher cognitive functions is largely unknown. In this study, we removed the ECM in the auditory cortex of adult Mongolian gerbils during specific phases of cortex-dependent auditory relearning, which was induced by the contingency reversal of a frequency-modulated tone discrimination, a task requiring high behavioral flexibility. We found that ECM removal promoted a significant increase in relearning performance, without erasing already establishedthat is, learned-capacities when continuing discrimination training. The cognitive flexibility required for reversal learning of previously acquired behavioral habits, commonly understood to mainly rely on frontostriatal circuits, was enhanced by promoting synaptic plasticity via ECM removal within the sensory cortex. Our findings further suggest experimental modulation of the cortical ECM as a tool to open short-term windows of enhanced activitydependent reorganization allowing for guided neuroplasticity.chondroitin sulfate proteoglycan | hyaluronidase | perineuronal net | intracortical microinjection | strategy change S tructural remodeling and stabilization of synaptic networks are key mechanisms underlying learning in the adult brain. During early life, high structural and functional plasticity is required for the experience-shaped development of basic neuronal circuits (1). With brain maturation, juvenile plasticity of so-called critical or sensitive periods is decreased and is accompanied by the appearance of the brain's extracellular matrix (ECM) and its specialized compact form named "perineuronal net" (PNN) enwrappping cell bodies and synaptic contacts (2, 3). Enzymatic degradation of the ECM in adult animals has been demonstrated to restore such forms of developmental (juvenile) plasticity with respect to topographical map plasticity in the visual cortex (4), fearresponse-mediating circuits in the amygdala (5), spinal cord injuries (6, 7), and song learning circuits of zebra finches (8). In addition, enzymatic ECM removal altered several forms of synaptic plasticity in vitro and in vivo (9-12). However, even though structural stability of networks acquired during developmental phases is essential for neuronal efficiency, mechanisms allowing synaptic remodeling are key events during learning and memory formation throughout life (13). We recently demonstrated that endogenous proteases moderately digesting specific components of the ECM are regulated in an activity-dependent manner (2, 14) and ECM removal modulates synaptic short-term plasticity by synaptic e...

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Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat

Cited by 123 publications

References 72 publications

Laminar and columnar auditory cortex in avian brain

Laminar and columnar auditory cortex in avian brain

Disruption of the perineuronal net in the hippocampus or medial prefrontal cortex impairs fear conditioning

Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex

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