Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário
In primates and carnivores, the primary visual cortex contains long-range selective horizontal connections which are thought to contribute to the perceptual grouping of local image elements according to their orientation, direction of movement and collinear alignment. These selective circuits cou...
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Conexões calosas Córtex visual primário Atividade neuronal de disparo Integração perceptiva visual CNPQ::OUTROS::CIENCIAS |
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Conexões calosas Córtex visual primário Atividade neuronal de disparo Integração perceptiva visual CNPQ::OUTROS::CIENCIAS Frota, Beatriz Carvalho Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário |
| description |
In primates and carnivores, the primary visual cortex contains long-range
selective horizontal connections which are thought to contribute to the perceptual
grouping of local image elements according to their orientation, direction of
movement and collinear alignment. These selective circuits could be also decisive in
maintaining biases in the ongoing cortical activity that condition neuronal responses
by facilitating the likely conjunctions of forms or movement trajectories before such a
stimulus arrives. Thus, ongoing functional interactions should reflect the selective
cortical connectivity. Close to the border of the primary visual cortex, these
connections extend through the corpus callosum with the same selectivity for
orientation, direction of movement and collinearity to link homotopic sites in the two
hemispheres and unify the image split in two halves at the vertical midline of the
visual field. Because of this central action of visual callosal connections, it is possible
to compare the ongoing and stimulus-evoked inter-hemispheric and
intra-hemispheric interactions, and investigate whether they represent shapes and
directions of movement crossing the vertical midline. To address the neuronal
signatures of those functional interactions we studied the activity of neurons
representing midline crossing stimuli in the two visual cortices by recording
simultaneously from 2 x 16 spatially separated electrodes. These electrodes were
placed into homotopic parts of the visual cortex, i.e. the transition zone between area
17 and 18, in cats (n = 4). In order to implant electrodes into cortical sites that are
directly or indirectly linked by the corpus callosum, we performed intrinsic signal
imaging to precisely define the areal border. Subsequently, we obtained extracellular
electrophysiological recordings of single unit spiking activity during grating and
natural visual stimulation designed to study integration. As an efficient measure of
functional interaction we used ongoing and stimulus-evoked coherence between
pairs of firing rates in the low-Gamma frequency band, focusing on pairs of neurons
with overlapping receptive fields. To restrict the analysis to optimally responding
neurons we applied a Sign test and a criterion of orientation- and direction selectivity.
We observed significant ongoing and evoked low Gamma band (30-59 Hz)
coherence in the majority of interhemispheric (n=131) and intra-hemispheric pairs
(n=132) of single units with overlapping RFs (at least in one stimulus condition), but with higher amplitudes between intra-hemispheric units. Intra-hemispherically, the
ongoing pairwise coherence decayed with cortical distance between neurons of the
same orientation preference (ISO) and peaked again at an interval of about 800μm
in accordance with the clustering of horizontal long-range connections linking sites of
iso-orientation preference. In accordance with the latter, both intra- and
interhemispheric ongoing and stimulus-evoked coherence was higher for pairs of
single units with the same orientation or direction selectivity (ISO) than with the
opposite selectivity (CROSS). Overall, horizontal gratings (± 45 degree) evoked
higher coherence than vertical ones (± 45 degree). Surprisingly, this bias was the
same for intra- and interhemispheric pairs. With natural scene stimulation,
intra-hemispheric coherence was higher for pairs of the opposite direction selectivity
(CROSSdir), in contrast to gratings, but for interhemispheric pairs of the same
direction selectivity (ISOdir). Also in contrast to gratings, coherences were higher for
directions of movement crossing (left, right) the vertical midline than for directions
running parallel to it (up and down). During grating and natural scene stimulation, we
observed both types of assemblies, either restricted to the population of
intra-hemispheric neurons or across the hemispheres. With gratings,
intra-hemispheric assemblies were significantly more often activated than
interhemispheric ones. However, similar to the bias in pairwise coherence,
interhemispheric assemblies were significantly more often activated during
stimulation with horizontal gratings (± 45 degree) than with vertical ones.
Interestingly, with natural scene stimulation intra- and interhemispheric assemblies
do neither differ in absolute activation rate nor stimulus selectivity indicating that
under these conditions both populations are functionally linked within one horizontal
circuit which includes both hemispheres. In conclusion, we confirm that both ongoing
and stimulus-driven activity of long-range intra- and interhemispheric networks
reflects the selectivity of long-range axons to link neurons of similar response
properties over longer distances. Selective neuronal interactions can be seen in
both, pairwise coherence activity in the low-Gamma range and in the activity of
simultaneously active populations of neurons spanning one or both visual cortices.
The results are compatible with the interpretation that those connections serve to
anticipate and mediate likely grouping operations between neurons representing the
vertical meridian, such as those caused by crossing movements, frequently
observed in natural scenes, or shapes such as in gratings. They also confirm that intra- and interhemispheric connections in the primary visual cortex are most likely not functionally separate circuits but rather form one horizontal network continuing through the corpus callosum. |
| author2 |
Schmidt, Kerstin Erika |
| author_facet |
Schmidt, Kerstin Erika Frota, Beatriz Carvalho |
| format |
doctoralThesis |
| author |
Frota, Beatriz Carvalho |
| author_sort |
Frota, Beatriz Carvalho |
| title |
Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário |
| title_short |
Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário |
| title_full |
Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário |
| title_fullStr |
Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário |
| title_full_unstemmed |
Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário |
| title_sort |
caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário |
| publisher |
Universidade Federal do Rio Grande do Norte |
| publishDate |
2024 |
| url |
https://repositorio.ufrn.br/handle/123456789/57903 |
| work_keys_str_mv |
AT frotabeatrizcarvalho caracterizacaofuncionaldepareseassembleiasdeneuroniosintraeinterhemisfericosnocortexvisualprimario |
| _version_ |
1797696554928177152 |
| spelling |
ri-123456789-579032024-03-19T22:27:31Z Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário Frota, Beatriz Carvalho Schmidt, Kerstin Erika http://lattes.cnpq.br/2930959007397988 http://lattes.cnpq.br/4902752912395893 Ocazionez, Sérgio Andrés Conde http://lattes.cnpq.br/7159531395590165 Ocazionez, Sérgio Andrés Conde Tort, Adriano Bretanha Lopes https://orcid.org/0000-0002-9877-7816 http://lattes.cnpq.br/3181888189086405 Takahashi, Daniel Yasumasa Santos, Natanael Antônio dos Conexões calosas Córtex visual primário Atividade neuronal de disparo Integração perceptiva visual CNPQ::OUTROS::CIENCIAS In primates and carnivores, the primary visual cortex contains long-range selective horizontal connections which are thought to contribute to the perceptual grouping of local image elements according to their orientation, direction of movement and collinear alignment. These selective circuits could be also decisive in maintaining biases in the ongoing cortical activity that condition neuronal responses by facilitating the likely conjunctions of forms or movement trajectories before such a stimulus arrives. Thus, ongoing functional interactions should reflect the selective cortical connectivity. Close to the border of the primary visual cortex, these connections extend through the corpus callosum with the same selectivity for orientation, direction of movement and collinearity to link homotopic sites in the two hemispheres and unify the image split in two halves at the vertical midline of the visual field. Because of this central action of visual callosal connections, it is possible to compare the ongoing and stimulus-evoked inter-hemispheric and intra-hemispheric interactions, and investigate whether they represent shapes and directions of movement crossing the vertical midline. To address the neuronal signatures of those functional interactions we studied the activity of neurons representing midline crossing stimuli in the two visual cortices by recording simultaneously from 2 x 16 spatially separated electrodes. These electrodes were placed into homotopic parts of the visual cortex, i.e. the transition zone between area 17 and 18, in cats (n = 4). In order to implant electrodes into cortical sites that are directly or indirectly linked by the corpus callosum, we performed intrinsic signal imaging to precisely define the areal border. Subsequently, we obtained extracellular electrophysiological recordings of single unit spiking activity during grating and natural visual stimulation designed to study integration. As an efficient measure of functional interaction we used ongoing and stimulus-evoked coherence between pairs of firing rates in the low-Gamma frequency band, focusing on pairs of neurons with overlapping receptive fields. To restrict the analysis to optimally responding neurons we applied a Sign test and a criterion of orientation- and direction selectivity. We observed significant ongoing and evoked low Gamma band (30-59 Hz) coherence in the majority of interhemispheric (n=131) and intra-hemispheric pairs (n=132) of single units with overlapping RFs (at least in one stimulus condition), but with higher amplitudes between intra-hemispheric units. Intra-hemispherically, the ongoing pairwise coherence decayed with cortical distance between neurons of the same orientation preference (ISO) and peaked again at an interval of about 800μm in accordance with the clustering of horizontal long-range connections linking sites of iso-orientation preference. In accordance with the latter, both intra- and interhemispheric ongoing and stimulus-evoked coherence was higher for pairs of single units with the same orientation or direction selectivity (ISO) than with the opposite selectivity (CROSS). Overall, horizontal gratings (± 45 degree) evoked higher coherence than vertical ones (± 45 degree). Surprisingly, this bias was the same for intra- and interhemispheric pairs. With natural scene stimulation, intra-hemispheric coherence was higher for pairs of the opposite direction selectivity (CROSSdir), in contrast to gratings, but for interhemispheric pairs of the same direction selectivity (ISOdir). Also in contrast to gratings, coherences were higher for directions of movement crossing (left, right) the vertical midline than for directions running parallel to it (up and down). During grating and natural scene stimulation, we observed both types of assemblies, either restricted to the population of intra-hemispheric neurons or across the hemispheres. With gratings, intra-hemispheric assemblies were significantly more often activated than interhemispheric ones. However, similar to the bias in pairwise coherence, interhemispheric assemblies were significantly more often activated during stimulation with horizontal gratings (± 45 degree) than with vertical ones. Interestingly, with natural scene stimulation intra- and interhemispheric assemblies do neither differ in absolute activation rate nor stimulus selectivity indicating that under these conditions both populations are functionally linked within one horizontal circuit which includes both hemispheres. In conclusion, we confirm that both ongoing and stimulus-driven activity of long-range intra- and interhemispheric networks reflects the selectivity of long-range axons to link neurons of similar response properties over longer distances. Selective neuronal interactions can be seen in both, pairwise coherence activity in the low-Gamma range and in the activity of simultaneously active populations of neurons spanning one or both visual cortices. The results are compatible with the interpretation that those connections serve to anticipate and mediate likely grouping operations between neurons representing the vertical meridian, such as those caused by crossing movements, frequently observed in natural scenes, or shapes such as in gratings. They also confirm that intra- and interhemispheric connections in the primary visual cortex are most likely not functionally separate circuits but rather form one horizontal network continuing through the corpus callosum. Em primatas e carnívoros, o córtex visual primário contém conexões horizontais seletivas de longo alcance que contribuem para o agrupamento de elementos locais da imagem de acordo com sua orientação, direção do movimento e alinhamento colinear. Esses circuitos seletivos também podem ser decisivos para manter vieses na atividade cortical espontânea que condicionam as respostas neuronais ao facilitar as prováveis conjunções de formas ou trajetórias de movimento antes que tal estímulo chegue. Assim, as interações funcionais em curso devem refletir a topografia seletiva das conexões. Perto da borda do córtex visual primário, essas conexões se estendem através do corpo caloso com a mesma seletividade para orientação, direção do movimento e colinearidade para ligar locais homotópicos nos dois hemisférios e unificar a imagem dividida em duas metades na linha média vertical do campo visual. Devido a essa ação central das conexões calosas visuais, é possível comparar as interações inter-hemisféricas e intra-hemisféricas espontâneas e evocadas pelo mesmo estímulo e investigar se elas representam formas e direções de movimento que cruzam a linha média vertical. Para abordar as assinaturas neuronais dessas interações funcionais, estudamos a atividade dos neurônios que representam estímulos que cruzam a linha média nos dois córtices visuais, registrando simultaneamente de 2 x 16 eletrodos separados espacialmente. Esses eletrodos foram colocados em partes homotópicas do córtex visual, ou seja, a zona de transição entre a área 17 e 18, em gatos (n = 4). Para implantar eletrodos em locais corticais direta ou indiretamente ligados pelo corpo caloso, realizamos imagens de sinal intrínseco para definir com precisão a área da borda. Posteriormente, obtivemos registros eletrofisiológicos extracelulares durante a estimulação visual com gratings e cenas naturais desenhados para estudar a integração. Como uma medida eficiente de interação funcional, usamos coerência espontânea e evocada por estímulo entre pares de taxas de disparo na banda de low-gamma, focando em pares de neurônios com campos receptivos sobrepostos. Para restringir a análise a neurônios com resposta otimizada, aplicamos um teste de sinal e um critério de seletividade de orientação e direção. Observamos coerência significativa da banda low-gamma espontânea e evocada (30-59 Hz) na maioria dos pares inter-hemisféricos (n=131) e intra-hemisféricos (n=132) de unidades únicas com RFs sobrepostos, mas com amplitudes maiores entre as unidades intra-hemisféricas. Dentro do mesmo hemisfério, a coerência decaiu com a distância cortical entre os neurônios da mesma preferência de orientação (ISO) e atingiu o pico novamente em um intervalo de cerca de 800 μm de acordo com o agrupamento de conexões horizontais de longo alcance. A coerência espontânea intra - e inter-hemisférica e a coerência evocada por estímulos foram maiores para pares com seletividade a mesma orientação ou direção de movimento (ISO) do que com a seletividade oposta (CROSS). No geral, a horizontal (± 45 graus) evocou maior coerência do que os gratings verticais (± 45 graus). Surpreendentemente, esse viés foi o mesmo para pares intra - e inter-hemisféricos. Com estimulação de cena natural, a coerência intra-hemisférica foi maior para pares de seletividade de direção oposta (CROSSdir), em contraste dos gratings, mas para pares inter-hemisféricos de seletividade de mesma direção (ISOdir). Também em contraste aos gratings, as coerências foram maiores para direções de movimento cruzando (para esquerda, para direita) a linha média vertical do que para direções paralelas a ela (para cima e para baixo). Durante a estimulação com gratings e cenas naturais, observamos ambos os tipos de assembleias, tanto restritas à população de neurônios intra-hemisféricos quanto inter-hemisféricos. Com gratings, as assembleias intra-hemisféricas foram significativamente mais frequentemente ativadas do que as inter-hemisféricas. No entanto, semelhante ao viés na coerência, a estimulação com gratings horizontais (± 45 graus) produziu taxas de ativação das assembleias inter-hemisféricas significativamente maiores do que com as verticais. Curiosamente, com a estimulação de cena natural, as assembleias intra e inter-hemisféricas não diferem na taxa de ativação nem na seletividade ao estímulo, indicando que, nessas condições, ambas as populações estão funcionalmente interconectadas em um único circuito horizontal que inclui os dois hemisférios. Em conclusão, confirmamos que a atividade espontânea e evocada por estímulos de redes intra - e inter-hemisféricas reflete a seletividade de axônios de longo alcance para ligar neurônios de propriedades de resposta semelhantes em distâncias mais longas. As interações neuronais seletivas podem ser vistas tanto na atividade de coerência na faixa de low-gamma quanto na atividade de populações simultaneamente ativas de neurônios abrangendo um ou ambos os córtices visuais. Os resultados são compatíveis com a interpretação de que essas conexões servem para antecipar e mediar prováveis operações de agrupamento entre neurônios que representam o meridiano vertical, como aquelas causadas por movimentos de cruzamento, frequentemente observados em cenas naturais, ou formas como o caso em gratings. Eles também confirmam que as conexões intra - e inter-hemisféricas dentro da representação do campo visual central no córtex visual primário provavelmente não são circuitos com funções distintas, mas formam uma única rede horizontal que continua até o outro hemisfério através do corpo caloso. 2024-03-19T22:26:39Z 2024-03-19T22:26:39Z 2023-06-12 doctoralThesis FROTA, Beatriz Carvalho. Caracterização funcional de pares e assembleias de neurônios intra- e inter-hemisféricos no córtex visual primário. Orientadora: Dra. Kerstin Erika Schmidt. 2023. 197f. Tese (Doutorado em Neurociências) - Instituto do Cérebro, Universidade Federal do Rio Grande do Norte, Natal, 2023. https://repositorio.ufrn.br/handle/123456789/57903 pt_BR Acesso Aberto application/pdf Universidade Federal do Rio Grande do Norte Brasil UFRN PROGRAMA DE PÓS-GRADUAÇÃO EM NEUROCIÊNCIAS |