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Neurophysiological correlates of object recognition in the dorsal subiculum.

Chang EH, Huerta PT - Front Behav Neurosci (2012)

Bottom Line: Furthermore, single-unit recordings revealed that DS cells did not exhibit phase-locked firing to theta and differed from CA1 place cells in that they had multiple peaks of spatially selective firing.We also detected DS units that were responsive specifically to novel object exploration, indicating that a subset of DS neurons were tuned to novelty during the NOR task.We have thus identified clear neurophysiological correlates for recognition within the DS, at the network and single-unit levels, strongly suggesting that it participates in encoding recognition-related signals.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Immune and Neural Networks, Center for Biomedical Science, The Feinstein Institute for Medical Research, North Shore-LIJ Health System, Manhasset NY, USA.

ABSTRACT
The medial temporal lobe (MTL) encompasses a network of interconnected cortical areas that is considered the neural substrate for some types of memory, such as spatial, episodic, recognition, and associative memory. Within the MTL, the subiculum has been well characterized in terms of its connectivity and structure, but its functional role remains elusive. A long-held view is that the subiculum is mainly involved in spatial encoding because it exhibits spatially selective firing and receives prominent projections from the CA1 field, which is an essential substrate for spatial memory. However, the dorsal subiculum (DS) is also reciprocally connected to the perirhinal and postrhinal cortices, which are critically involved in recognition memory. This connectivity pattern suggests that DS might encode not only spatial signals but also recognition signals. Here, we examined this hypothesis by recording with multi-electrodes in DS and CA1 of freely behaving mice, as they performed the novel object recognition (NOR) task. Analysis of network oscillations revealed that theta power was significantly higher in DS when mice explored novel objects as compared to familiar objects and that this theta modulation was absent in CA1. We also found significant differences in coherence between DS and CA1, in the theta and gamma bands, depending on whether mice examined objects or engaged in spatial exploration. Furthermore, single-unit recordings revealed that DS cells did not exhibit phase-locked firing to theta and differed from CA1 place cells in that they had multiple peaks of spatially selective firing. We also detected DS units that were responsive specifically to novel object exploration, indicating that a subset of DS neurons were tuned to novelty during the NOR task. We have thus identified clear neurophysiological correlates for recognition within the DS, at the network and single-unit levels, strongly suggesting that it participates in encoding recognition-related signals.

No MeSH data available.


Related in: MedlinePlus

Spatial selectivity and object responsiveness of dorsal subicular neurons. (A)Top left, action potentials from three subicular neurons are shown in red, blue, and green. Top right, the spikes are isolated by principal component clustering, of which two projections (labeled PC1 and PC2) are shown. Bottom, autocorrelogram for a principal neuron recorded during a choice trial. (B)Left, peri-event histograms for two novelty-responsive DS neurons, one on each row, during exploration of familiar and novel objects. Dashed lines indicate the onset of object exploration. Right, Plot of the normalized firing rate (mean ± SEM), 500–1000 ms after the start of exploration of familiar and novel objects for this subset of DS neurons. **p < 0.005 (t-test). (C) Firing rate maps of four DS neurons during the sequential stages of the NOR task showing broad place fields with several peaks of firing within the behavioral context. In these top views of the square chamber (30 cm on the side), gray circles indicate the locations of the objects. The color scales (at left of each map) specify the firing rates (spikes per sec) for the units. It is clear that subicular place cells exhibit spatial selectivity that does not appear to be modulated by the presence of objects nor their degree of novelty.
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Figure 8: Spatial selectivity and object responsiveness of dorsal subicular neurons. (A)Top left, action potentials from three subicular neurons are shown in red, blue, and green. Top right, the spikes are isolated by principal component clustering, of which two projections (labeled PC1 and PC2) are shown. Bottom, autocorrelogram for a principal neuron recorded during a choice trial. (B)Left, peri-event histograms for two novelty-responsive DS neurons, one on each row, during exploration of familiar and novel objects. Dashed lines indicate the onset of object exploration. Right, Plot of the normalized firing rate (mean ± SEM), 500–1000 ms after the start of exploration of familiar and novel objects for this subset of DS neurons. **p < 0.005 (t-test). (C) Firing rate maps of four DS neurons during the sequential stages of the NOR task showing broad place fields with several peaks of firing within the behavioral context. In these top views of the square chamber (30 cm on the side), gray circles indicate the locations of the objects. The color scales (at left of each map) specify the firing rates (spikes per sec) for the units. It is clear that subicular place cells exhibit spatial selectivity that does not appear to be modulated by the presence of objects nor their degree of novelty.

Mentions: As already reported by others (Barnes et al., 1990; Sharp and Green, 1994; Gigg et al., 2000; Anderson and O'Mara, 2004; Brontons-Mas et al., 2010), it was significantly harder to record well-isolated DS units, as compared to concomitantly recorded CA1 units. Over 96 recording sessions, we obtained a total of 38 DS units, 28 of which were identified as principal cells and 10 as interneurons on the basis of their firing rates, autocorrelograms, and spike widths (Figure 8A, Table 1). By comparison, we recorded a total of 72 CA1 units, 51 of which were classified as pyramidal cells and 21 as interneurons. We found that the majority of the subicular neurons (32 of 38, ~84%) were not responsive to objects, meaning that they did not change their firing rate (increase or decrease) as a function of the mouse exploring either a novel or a familiar object. However, we were able to isolate a subset of DS principal neurons (6 of 28, 21.4%) that were specifically modulated during the exploration of novel objects. Figure 8B shows representative examples of these novelty-responsive subicular cells and their firing rates in relation to approaching a novel object or a familiar object. There was a marked increase in spiking after the onset of novel object exploration, which peaked at 796.4 ms after onset, and which was completely absent during the exploration of familiar objects. Analysis of multiple epochs showed that this was a statistically robust phenomenon. We examined the firing in the interval of 500–1000 ms after the start of object exploration, and found that the novelty-responsive DS cells had a significantly higher firing rate for novel objects as compared to familiar objects (Figure 8B, right) [novel = 165 ± 19%, familiar = 98 ± 6%, n = 211 visits; t-test, t = 3.46, p < 0.005]. These particular DS neurons may be critical within a recognition memory neural system, given their heightened responsiveness to novel stimuli.


Neurophysiological correlates of object recognition in the dorsal subiculum.

Chang EH, Huerta PT - Front Behav Neurosci (2012)

Spatial selectivity and object responsiveness of dorsal subicular neurons. (A)Top left, action potentials from three subicular neurons are shown in red, blue, and green. Top right, the spikes are isolated by principal component clustering, of which two projections (labeled PC1 and PC2) are shown. Bottom, autocorrelogram for a principal neuron recorded during a choice trial. (B)Left, peri-event histograms for two novelty-responsive DS neurons, one on each row, during exploration of familiar and novel objects. Dashed lines indicate the onset of object exploration. Right, Plot of the normalized firing rate (mean ± SEM), 500–1000 ms after the start of exploration of familiar and novel objects for this subset of DS neurons. **p < 0.005 (t-test). (C) Firing rate maps of four DS neurons during the sequential stages of the NOR task showing broad place fields with several peaks of firing within the behavioral context. In these top views of the square chamber (30 cm on the side), gray circles indicate the locations of the objects. The color scales (at left of each map) specify the firing rates (spikes per sec) for the units. It is clear that subicular place cells exhibit spatial selectivity that does not appear to be modulated by the presence of objects nor their degree of novelty.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 8: Spatial selectivity and object responsiveness of dorsal subicular neurons. (A)Top left, action potentials from three subicular neurons are shown in red, blue, and green. Top right, the spikes are isolated by principal component clustering, of which two projections (labeled PC1 and PC2) are shown. Bottom, autocorrelogram for a principal neuron recorded during a choice trial. (B)Left, peri-event histograms for two novelty-responsive DS neurons, one on each row, during exploration of familiar and novel objects. Dashed lines indicate the onset of object exploration. Right, Plot of the normalized firing rate (mean ± SEM), 500–1000 ms after the start of exploration of familiar and novel objects for this subset of DS neurons. **p < 0.005 (t-test). (C) Firing rate maps of four DS neurons during the sequential stages of the NOR task showing broad place fields with several peaks of firing within the behavioral context. In these top views of the square chamber (30 cm on the side), gray circles indicate the locations of the objects. The color scales (at left of each map) specify the firing rates (spikes per sec) for the units. It is clear that subicular place cells exhibit spatial selectivity that does not appear to be modulated by the presence of objects nor their degree of novelty.
Mentions: As already reported by others (Barnes et al., 1990; Sharp and Green, 1994; Gigg et al., 2000; Anderson and O'Mara, 2004; Brontons-Mas et al., 2010), it was significantly harder to record well-isolated DS units, as compared to concomitantly recorded CA1 units. Over 96 recording sessions, we obtained a total of 38 DS units, 28 of which were identified as principal cells and 10 as interneurons on the basis of their firing rates, autocorrelograms, and spike widths (Figure 8A, Table 1). By comparison, we recorded a total of 72 CA1 units, 51 of which were classified as pyramidal cells and 21 as interneurons. We found that the majority of the subicular neurons (32 of 38, ~84%) were not responsive to objects, meaning that they did not change their firing rate (increase or decrease) as a function of the mouse exploring either a novel or a familiar object. However, we were able to isolate a subset of DS principal neurons (6 of 28, 21.4%) that were specifically modulated during the exploration of novel objects. Figure 8B shows representative examples of these novelty-responsive subicular cells and their firing rates in relation to approaching a novel object or a familiar object. There was a marked increase in spiking after the onset of novel object exploration, which peaked at 796.4 ms after onset, and which was completely absent during the exploration of familiar objects. Analysis of multiple epochs showed that this was a statistically robust phenomenon. We examined the firing in the interval of 500–1000 ms after the start of object exploration, and found that the novelty-responsive DS cells had a significantly higher firing rate for novel objects as compared to familiar objects (Figure 8B, right) [novel = 165 ± 19%, familiar = 98 ± 6%, n = 211 visits; t-test, t = 3.46, p < 0.005]. These particular DS neurons may be critical within a recognition memory neural system, given their heightened responsiveness to novel stimuli.

Bottom Line: Furthermore, single-unit recordings revealed that DS cells did not exhibit phase-locked firing to theta and differed from CA1 place cells in that they had multiple peaks of spatially selective firing.We also detected DS units that were responsive specifically to novel object exploration, indicating that a subset of DS neurons were tuned to novelty during the NOR task.We have thus identified clear neurophysiological correlates for recognition within the DS, at the network and single-unit levels, strongly suggesting that it participates in encoding recognition-related signals.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Immune and Neural Networks, Center for Biomedical Science, The Feinstein Institute for Medical Research, North Shore-LIJ Health System, Manhasset NY, USA.

ABSTRACT
The medial temporal lobe (MTL) encompasses a network of interconnected cortical areas that is considered the neural substrate for some types of memory, such as spatial, episodic, recognition, and associative memory. Within the MTL, the subiculum has been well characterized in terms of its connectivity and structure, but its functional role remains elusive. A long-held view is that the subiculum is mainly involved in spatial encoding because it exhibits spatially selective firing and receives prominent projections from the CA1 field, which is an essential substrate for spatial memory. However, the dorsal subiculum (DS) is also reciprocally connected to the perirhinal and postrhinal cortices, which are critically involved in recognition memory. This connectivity pattern suggests that DS might encode not only spatial signals but also recognition signals. Here, we examined this hypothesis by recording with multi-electrodes in DS and CA1 of freely behaving mice, as they performed the novel object recognition (NOR) task. Analysis of network oscillations revealed that theta power was significantly higher in DS when mice explored novel objects as compared to familiar objects and that this theta modulation was absent in CA1. We also found significant differences in coherence between DS and CA1, in the theta and gamma bands, depending on whether mice examined objects or engaged in spatial exploration. Furthermore, single-unit recordings revealed that DS cells did not exhibit phase-locked firing to theta and differed from CA1 place cells in that they had multiple peaks of spatially selective firing. We also detected DS units that were responsive specifically to novel object exploration, indicating that a subset of DS neurons were tuned to novelty during the NOR task. We have thus identified clear neurophysiological correlates for recognition within the DS, at the network and single-unit levels, strongly suggesting that it participates in encoding recognition-related signals.

No MeSH data available.


Related in: MedlinePlus