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1.
Neuron ; 112(17): 2938-2954.e6, 2024 Sep 04.
Artículo en Inglés | MEDLINE | ID: mdl-38964330

RESUMEN

Neuronal activity plays a critical role in the maturation of circuits that propagate sensory information into the brain. How widely does early activity regulate circuit maturation across the developing brain? Here, we used targeted recombination in active populations (TRAP) to perform a brain-wide survey for prenatally active neurons in mice and identified the piriform cortex as an abundantly TRAPed region. Whole-cell recordings in neonatal slices revealed preferential interconnectivity within embryonically TRAPed piriform neurons and their enhanced synaptic connectivity with other piriform neurons. In vivo Neuropixels recordings in neonates demonstrated that embryonically TRAPed piriform neurons exhibit broad functional connectivity within piriform and lead spontaneous synchronized population activity during a transient neonatal period, when recurrent connectivity is strengthening. Selectively activating or silencing these neurons in neonates enhanced or suppressed recurrent synaptic strength, respectively. Thus, embryonically TRAPed piriform neurons represent an interconnected hub-like population whose activity promotes recurrent connectivity in early development.


Asunto(s)
Neuronas , Corteza Piriforme , Animales , Ratones , Neuronas/fisiología , Animales Recién Nacidos , Técnicas de Placa-Clamp , Femenino , Red Nerviosa/fisiología
2.
bioRxiv ; 2024 May 09.
Artículo en Inglés | MEDLINE | ID: mdl-38766173

RESUMEN

Neuronal activity plays a critical role in the maturation of circuits that propagate sensory information into the brain. How widely does early activity regulate circuit maturation across the developing brain? Here, we used Targeted Recombination in Active Populations (TRAP) to perform a brain-wide survey for prenatally active neurons in mice and identified the piriform cortex as an abundantly TRAPed region. Whole-cell recordings in neonatal slices revealed preferential interconnectivity within embryonically TRAPed piriform neurons and their enhanced synaptic connectivity with other piriform neurons. In vivo Neuropixels recordings in neonates demonstrated that embryonically TRAPed piriform neurons exhibit broad functional connectivity within piriform and lead spontaneous synchronized population activity during a transient neonatal period, when recurrent connectivity is strengthening. Selectively activating or silencing of these neurons in neonates enhanced or suppressed recurrent synaptic strength, respectively. Thus, embryonically TRAPed piriform neurons represent an interconnected hub-like population whose activity promotes recurrent connectivity in early development.

3.
bioRxiv ; 2024 Jul 01.
Artículo en Inglés | MEDLINE | ID: mdl-38496526

RESUMEN

In natural odor environments, odor travels in plumes. Odor concentration dynamics change in characteristic ways across the width and length of a plume. Thus, spatiotemporal dynamics of plumes have informative features for animals navigating to an odor source. Population activity in the olfactory bulb (OB) has been shown to follow odor concentration across plumes to a moderate degree (Lewis et al., 2021). However, it is unknown whether the ability to follow plume dynamics is driven by individual cells or whether it emerges at the population level. Previous research has explored the responses of individual OB cells to isolated features of plumes, but it is difficult to adequately sample the full feature space of plumes as it is still undetermined which features navigating mice employ during olfactory guided search. Here we released odor from an upwind odor source and simultaneously recorded both odor concentration dynamics and cellular response dynamics in awake, head-fixed mice. We found that longer timescale features of odor concentration dynamics were encoded at both the cellular and population level. At the cellular level, responses were elicited at the beginning of the plume for each trial, signaling plume onset. Plumes with high odor concentration elicited responses at the end of the plume, signaling plume offset. Although cellular level tracking of plume dynamics was observed to be weak, we found that at the population level, OB activity distinguished whiffs and blanks (accurately detected odor presence versus absence) throughout the duration of a plume. Even ~20 OB cells were enough to accurately discern odor presence throughout a plume. Our findings indicate that the full range of odor concentration dynamics and high frequency fluctuations are not encoded by OB spiking activity. Instead, relatively lower-frequency temporal features of plumes, such as plume onset, plume offset, whiffs, and blanks, are represented in the OB.

4.
Methods Mol Biol ; 2710: 209-221, 2023.
Artículo en Inglés | MEDLINE | ID: mdl-37688735

RESUMEN

Neural circuits consist of a myriad of distinct cell types, each with specific intrinsic properties and patterns of synaptic connectivity, which transform neural input and convey this information to downstream targets. Understanding how different features of an odor stimulus are encoded and relayed to their appropriate targets will require selective identification and manipulation of these different elements of the circuit. Here, we describe methods to obtain dense, extracellular electrophysiological recordings of odor-evoked activity in olfactory (piriform) cortex of awake, head-fixed mice, and optogenetic tools and procedures to identify genetically defined cell types within this circuit.


Asunto(s)
Corteza Olfatoria , Corteza Piriforme , Animales , Ratones , Vigilia , Optogenética , Olfato
5.
Curr Biol ; 33(7): R266-R269, 2023 04 10.
Artículo en Inglés | MEDLINE | ID: mdl-37040708

RESUMEN

Many cortical brain regions are spatially organized to optimize sensory representation. Such topographic maps have so far been elusive in the olfactory cortex. A high-throughput tracing study reveals that the neural circuits connecting olfactory regions are indeed topographically organized.


Asunto(s)
Mapeo Encefálico , Corteza Olfatoria , Animales , Ratones , Corteza Olfatoria/citología , Corteza Olfatoria/fisiología , Neurociencias/métodos , Neuronas/citología
6.
Elife ; 102021 12 16.
Artículo en Inglés | MEDLINE | ID: mdl-34913870

RESUMEN

Understanding how distinct neuron types in a neural circuit process and propagate information is essential for understanding what the circuit does and how it does it. The olfactory (piriform, PCx) cortex contains two main types of principal neurons, semilunar (SL) and superficial pyramidal (PYR) cells. SLs and PYRs have distinct morphologies, local connectivity, biophysical properties, and downstream projection targets. Odor processing in PCx is thought to occur in two sequential stages. First, SLs receive and integrate olfactory bulb input and then PYRs receive, transform, and transmit SL input. To test this model, we recorded from populations of optogenetically identified SLs and PYRs in awake, head-fixed mice. Notably, silencing SLs did not alter PYR odor responses, and SLs and PYRs exhibited differences in odor tuning properties and response discriminability that were consistent with their distinct embeddings within a sensory-associative cortex. Our results therefore suggest that SLs and PYRs form parallel channels for differentially processing odor information in and through PCx.


Asunto(s)
Ratones Transgénicos/fisiología , Neuronas/fisiología , Corteza Olfatoria/fisiología , Vías Olfatorias/fisiología , Células Piramidales/fisiología , Receptores Odorantes/fisiología , Olfato/fisiología , Animales , Masculino , Ratones
7.
Cell Rep ; 35(3): 109001, 2021 04 20.
Artículo en Inglés | MEDLINE | ID: mdl-33882304

RESUMEN

It is well established that seizures beget seizures, yet the cellular processes that underlie progressive epileptogenesis remain unclear. Here, we use optogenetics to briefly activate targeted populations of mouse piriform cortex (PCx) principal neurons in vivo. After just 3 or 4 days of stimulation, previously subconvulsive stimuli trigger massive, generalized seizures. Highly recurrent allocortices are especially prone to "optokindling." Optokindling upsets the balance of recurrent excitation and feedback inhibition. To understand how this balance is disrupted, we then selectively reactivate the same neurons in vitro. Surprisingly, we find no evidence of heterosynaptic potentiation; instead, we observe a marked, pathway-specific decrease in feedback inhibition. We find no loss of inhibitory interneurons; rather, decreased GABA synthesis in feedback inhibitory neurons appears to underlie weakened inhibition. Optokindling will allow precise identification of the molecular processes by which brain activity patterns can progressively and pathologically disrupt the balance of cortical excitation and inhibition.


Asunto(s)
Estimulación Eléctrica/métodos , Retroalimentación Sensorial , Corteza Piriforme/fisiopatología , Convulsiones/fisiopatología , Sinapsis/metabolismo , Ácido gamma-Aminobutírico/metabolismo , Animales , Electrodos Implantados , Potenciales Evocados/fisiología , Retroalimentación Fisiológica , Femenino , Masculino , Ratones , Neuronas/metabolismo , Neuronas/patología , Optogenética/métodos , Corteza Piriforme/metabolismo , Convulsiones/metabolismo , Técnicas Estereotáxicas , Sinapsis/patología , Transmisión Sináptica
8.
Curr Biol ; 30(22): 4548, 2020 Nov 16.
Artículo en Inglés | MEDLINE | ID: mdl-33202222
9.
J Neurosci ; 40(49): 9414-9425, 2020 12 02.
Artículo en Inglés | MEDLINE | ID: mdl-33115926

RESUMEN

Odors activate distributed ensembles of neurons within the piriform cortex, forming cortical representations of odor thought to be essential to olfactory learning and behaviors. This odor response is driven by direct input from the olfactory bulb, but is also shaped by a dense network of associative or intracortical inputs to piriform, which may enhance or constrain the cortical odor representation. With optogenetic techniques, it is possible to functionally isolate defined inputs to piriform cortex and assess their potential to activate or inhibit piriform pyramidal neurons. The anterior olfactory nucleus (AON) receives direct input from the olfactory bulb and sends an associative projection to piriform cortex that has potential roles in the state-dependent processing of olfactory behaviors. Here, we provide a detailed functional assessment of the AON afferents to piriform in male and female C57Bl/6J mice. We confirm that the AON forms glutamatergic excitatory synapses onto piriform pyramidal neurons; and while these inputs are not as strong as piriform recurrent collaterals, they are less constrained by disynaptic inhibition. Moreover, AON-to-piriform synapses contain a substantial NMDAR-mediated current that prolongs the synaptic response at depolarized potentials. These properties of limited inhibition and slow NMDAR-mediated currents result in strong temporal summation of AON inputs within piriform pyramidal neurons, and suggest that the AON could powerfully enhance activation of piriform neurons in response to odor.SIGNIFICANCE STATEMENT Odor information is transmitted from olfactory receptors to olfactory bulb, and then to piriform cortex, where ensembles of activated neurons form neural representations of the odor. While these ensembles are driven by primary bulbar afferents, and shaped by intracortical recurrent connections, the potential for another early olfactory area, the anterior olfactory nucleus (AON), to contribute to piriform activity is not known. Here, we use optogenetic circuit-mapping methods to demonstrate that AON inputs can significantly activate piriform neurons, as they are coupled to NMDAR currents and to relatively modest disynaptic inhibition. The AON may enhance the piriform odor response, encouraging further study to determine the states or behaviors through which AON potentiates the cortical response to odor.


Asunto(s)
Corteza Olfatoria/fisiología , Corteza Piriforme/fisiología , Olfato/fisiología , Sinapsis/fisiología , Animales , Femenino , Ácido Glutámico/fisiología , Masculino , Potenciales de la Membrana/fisiología , Ratones , Ratones Endogámicos C57BL , Neuronas Aferentes/fisiología , Odorantes , Bulbo Olfatorio/fisiología , Optogenética , Células Piramidales , Receptores de N-Metil-D-Aspartato/fisiología
10.
Curr Biol ; 30(20): R1279-R1281, 2020 10 19.
Artículo en Inglés | MEDLINE | ID: mdl-33080204

RESUMEN

Neuroscientists still are not sure what makes any two odors smell alike. A new study uses light to manipulate the sensory cells in our nose that respond to odors and reveals that both the timing and identity of activated cells influence odor perception.


Asunto(s)
Percepción Olfatoria , Lógica , Odorantes , Optogenética , Olfato
11.
Nature ; 584(7822): E38, 2020 Aug.
Artículo en Inglés | MEDLINE | ID: mdl-32782391

RESUMEN

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

12.
Nature ; 583(7815): 253-258, 2020 07.
Artículo en Inglés | MEDLINE | ID: mdl-32612230

RESUMEN

The cortex organizes sensory information to enable discrimination and generalization1-4. As systematic representations of chemical odour space have not yet been described in the olfactory cortex, it remains unclear how odour relationships are encoded to place chemically distinct but similar odours, such as lemon and orange, into perceptual categories, such as citrus5-7. Here, by combining chemoinformatics and multiphoton imaging in the mouse, we show that both the piriform cortex and its sensory inputs from the olfactory bulb represent chemical odour relationships through correlated patterns of activity. However, cortical odour codes differ from those in the bulb: cortex more strongly clusters together representations for related odours, selectively rewrites pairwise odour relationships, and better matches odour perception. The bulb-to-cortex transformation depends on the associative network originating within the piriform cortex, and can be reshaped by passive odour experience. Thus, cortex actively builds a structured representation of chemical odour space that highlights odour relationships; this representation is similar across individuals but remains plastic, suggesting a means through which the olfactory system can assign related odour cues to common and yet personalized percepts.


Asunto(s)
Odorantes/análisis , Corteza Olfatoria/anatomía & histología , Corteza Olfatoria/fisiología , Vías Olfatorias , Compuestos Orgánicos/análisis , Compuestos Orgánicos/química , Animales , Masculino , Ratones , Bulbo Olfatorio/citología , Bulbo Olfatorio/fisiología , Corteza Olfatoria/citología , Percepción Olfatoria/fisiología , Olfato
13.
Elife ; 92020 07 14.
Artículo en Inglés | MEDLINE | ID: mdl-32662420

RESUMEN

Pattern completion, or the ability to retrieve stable neural activity patterns from noisy or partial cues, is a fundamental feature of memory. Theoretical studies indicate that recurrently connected auto-associative or discrete attractor networks can perform this process. Although pattern completion and attractor dynamics have been observed in various recurrent neural circuits, the role recurrent circuitry plays in implementing these processes remains unclear. In recordings from head-fixed mice, we found that odor responses in olfactory bulb degrade under ketamine/xylazine anesthesia while responses immediately downstream, in piriform cortex, remain robust. Recurrent connections are required to stabilize cortical odor representations across states. Moreover, piriform odor representations exhibit attractor dynamics, both within and across trials, and these are also abolished when recurrent circuitry is eliminated. Here, we present converging evidence that recurrently-connected piriform populations stabilize sensory representations in response to degraded inputs, consistent with an auto-associative function for piriform cortex supported by recurrent circuitry.


Asunto(s)
Anestesia , Odorantes , Bulbo Olfatorio/fisiología , Vías Olfatorias/fisiología , Corteza Piriforme/fisiología , Animales , Ketamina/farmacología , Ratones , Bulbo Olfatorio/efectos de los fármacos , Vías Olfatorias/efectos de los fármacos , Corteza Piriforme/efectos de los fármacos , Sinapsis/fisiología , Xilazina/farmacología
14.
Curr Opin Neurobiol ; 64: 96-102, 2020 10.
Artículo en Inglés | MEDLINE | ID: mdl-32422571

RESUMEN

Olfaction facilitates a large variety of animal behaviors such as feeding, mating, and communication. Recent work has begun to reveal the logic of odor transformations that occur throughout the olfactory system to form the odor percept. In this review, we describe the coding principles and mechanisms by which the piriform cortex and other olfactory areas encode three key odor features: odor identity, intensity, and valence. We argue that the piriform cortex produces a multiplexed odor code that allows non-interfering representations of distinct features of the odor stimulus to facilitate odor recognition and learning, which ultimately drives behavior.


Asunto(s)
Corteza Piriforme , Animales , Aprendizaje , Odorantes , Vías Olfatorias , Percepción Olfatoria , Olfato
15.
Proc Natl Acad Sci U S A ; 117(12): 6708-6716, 2020 03 24.
Artículo en Inglés | MEDLINE | ID: mdl-32161123

RESUMEN

Antibodies against neuronal receptors and synaptic proteins are associated with a group of ill-defined central nervous system (CNS) autoimmune diseases termed autoimmune encephalitides (AE), which are characterized by abrupt onset of seizures and/or movement and psychiatric symptoms. Basal ganglia encephalitis (BGE), representing a subset of AE syndromes, is triggered in children by repeated group A Streptococcus (GAS) infections that lead to neuropsychiatric symptoms. We have previously shown that multiple GAS infections of mice induce migration of Th17 lymphocytes from the nose into the brain, causing blood-brain barrier (BBB) breakdown, extravasation of autoantibodies into the CNS, and loss of excitatory synapses within the olfactory bulb (OB). Whether these pathologies induce functional olfactory deficits, and the mechanistic role of Th17 lymphocytes, is unknown. Here, we demonstrate that, whereas loss of excitatory synapses in the OB is transient after multiple GAS infections, functional deficits in odor processing persist. Moreover, mice lacking Th17 lymphocytes have reduced BBB leakage, microglial activation, and antibody infiltration into the CNS, and have their olfactory function partially restored. Th17 lymphocytes are therefore critical for selective CNS entry of autoantibodies, microglial activation, and neural circuit impairment during postinfectious BGE.


Asunto(s)
Encéfalo/patología , Modelos Animales de Enfermedad , Encefalitis/etiología , Encefalomielitis Autoinmune Experimental/etiología , Enfermedad de Hashimoto/etiología , Trastornos del Olfato/etiología , Infecciones Estreptocócicas/complicaciones , Células Th17/inmunología , Animales , Autoanticuerpos/inmunología , Ganglios Basales/inmunología , Ganglios Basales/patología , Barrera Hematoencefálica , Encéfalo/inmunología , Encefalitis/metabolismo , Encefalitis/patología , Encefalomielitis Autoinmune Experimental/metabolismo , Encefalomielitis Autoinmune Experimental/patología , Femenino , Enfermedad de Hashimoto/metabolismo , Enfermedad de Hashimoto/patología , Ratones , Microglía/inmunología , Microglía/patología , Neuronas/inmunología , Neuronas/patología , Trastornos del Olfato/metabolismo , Trastornos del Olfato/patología , Percepción Olfatoria , Streptococcus pyogenes/fisiología , Linfocitos T Reguladores/inmunología , Linfocitos T Reguladores/patología , Células Th17/patología
16.
Science ; 361(6407)2018 09 14.
Artículo en Inglés | MEDLINE | ID: mdl-30213885

RESUMEN

Animals rely on olfaction to find food, attract mates, and avoid predators. To support these behaviors, they must be able to identify odors across different odorant concentrations. The neural circuit operations that implement this concentration invariance remain unclear. We found that despite concentration-dependence in the olfactory bulb (OB), representations of odor identity were preserved downstream, in the piriform cortex (PCx). The OB cells responding earliest after inhalation drove robust responses in sparse subsets of PCx neurons. Recurrent collateral connections broadcast their activation across the PCx, recruiting global feedback inhibition that rapidly truncated and suppressed cortical activity for the remainder of the sniff, discounting the impact of slower, concentration-dependent OB inputs. Eliminating recurrent collateral output amplified PCx odor responses rendered the cortex steeply concentration-dependent and abolished concentration-invariant identity decoding.


Asunto(s)
Vías Olfatorias/fisiología , Percepción Olfatoria , Corteza Piriforme/fisiología , Olfato/fisiología , Animales , Retroalimentación Fisiológica , Ratones , Odorantes/análisis , Bulbo Olfatorio/fisiología
17.
Elife ; 72018 03 29.
Artículo en Inglés | MEDLINE | ID: mdl-29595470

RESUMEN

Different coding strategies are used to represent odor information at various stages of the mammalian olfactory system. A temporal latency code represents odor identity in olfactory bulb (OB), but this temporal information is discarded in piriform cortex (PCx) where odor identity is instead encoded through ensemble membership. We developed a spiking PCx network model to understand how this transformation is implemented. In the model, the impact of OB inputs activated earliest after inhalation is amplified within PCx by diffuse recurrent collateral excitation, which then recruits strong, sustained feedback inhibition that suppresses the impact of later-responding glomeruli. We model increasing odor concentrations by decreasing glomerulus onset latencies while preserving their activation sequences. This produces a multiplexed cortical odor code in which activated ensembles are robust to concentration changes while concentration information is encoded through population synchrony. Our model demonstrates how PCx circuitry can implement multiplexed ensemble-identity/temporal-concentration odor coding.


Asunto(s)
Modelos Neurológicos , Odorantes , Percepción Olfatoria , Corteza Piriforme/fisiología , Potenciales de Acción , Animales , Electroencefalografía , Femenino , Masculino , Ratones , Tiempo
18.
Curr Biol ; 28(1): R23-R25, 2018 01 08.
Artículo en Inglés | MEDLINE | ID: mdl-29316416

RESUMEN

A new study reports unsupervised, experience-dependent reorganization, but not stabilization, of neural odor representations in the zebrafish olfactory system.


Asunto(s)
Odorantes , Pez Cebra , Animales , Aprendizaje , Plasticidad Neuronal , Corteza Olfatoria
19.
Elife ; 62017 05 10.
Artículo en Inglés | MEDLINE | ID: mdl-28489003

RESUMEN

Olfactory perception and behaviors critically depend on the ability to identify an odor across a wide range of concentrations. Here, we use calcium imaging to determine how odor identity is encoded in olfactory cortex. We find that, despite considerable trial-to-trial variability, odor identity can accurately be decoded from ensembles of co-active neurons that are distributed across piriform cortex without any apparent spatial organization. However, piriform response patterns change substantially over a 100-fold change in odor concentration, apparently degrading the population representation of odor identity. We show that this problem can be resolved by decoding odor identity from a subpopulation of concentration-invariant piriform neurons. These concentration-invariant neurons are overrepresented in piriform cortex but not in olfactory bulb mitral and tufted cells. We therefore propose that distinct perceptual features of odors are encoded in independent subnetworks of neurons in the olfactory cortex.


Asunto(s)
Neuronas/fisiología , Odorantes , Percepción Olfatoria , Corteza Piriforme/fisiología , Animales , Señalización del Calcio , Ratones , Modelos Neurológicos , Imagen Óptica
20.
Elife ; 62017 04 05.
Artículo en Inglés | MEDLINE | ID: mdl-28379135

RESUMEN

The ability to represent both stimulus identity and intensity is fundamental for perception. Using large-scale population recordings in awake mice, we find distinct coding strategies facilitate non-interfering representations of odor identity and intensity in piriform cortex. Simply knowing which neurons were activated is sufficient to accurately represent odor identity, with no additional information about identity provided by spike time or spike count. Decoding analyses indicate that cortical odor representations are not sparse. Odorant concentration had no systematic effect on spike counts, indicating that rate cannot encode intensity. Instead, odor intensity can be encoded by temporal features of the population response. We found a subpopulation of rapid, largely concentration-invariant responses was followed by another population of responses whose latencies systematically decreased at higher concentrations. Cortical inhibition transforms olfactory bulb output to sharpen these dynamics. Our data therefore reveal complementary coding strategies that can selectively represent distinct features of a stimulus.


Asunto(s)
Neuronas/fisiología , Odorantes , Percepción Olfatoria , Corteza Piriforme/fisiología , Potenciales de Acción , Animales , Ratones
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