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Distributed encoding of spatial and object categories in primate hippocampal microcircuits.

Opris I, Santos LM, Gerhardt GA, Song D, Berger TW, Hampson RE, Deadwyler SA - Front Neurosci (2015)

Bottom Line: The primate hippocampus plays critical roles in the encoding, representation, categorization and retrieval of cognitive information.Four nonhuman primates were trained in a delayed-match-to-sample (DMS) task while multi-neuron activity was simultaneously recorded from the CA1 and CA3 hippocampal cell fields.The results show differential encoding of spatial location and categorization of images presented as relevant stimuli in the task.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Pharmacology, Wake Forest University School of Medicine Winston-Salem, NC, USA.

ABSTRACT
The primate hippocampus plays critical roles in the encoding, representation, categorization and retrieval of cognitive information. Such cognitive abilities may use the transformational input-output properties of hippocampal laminar microcircuitry to generate spatial representations and to categorize features of objects, images, and their numeric characteristics. Four nonhuman primates were trained in a delayed-match-to-sample (DMS) task while multi-neuron activity was simultaneously recorded from the CA1 and CA3 hippocampal cell fields. The results show differential encoding of spatial location and categorization of images presented as relevant stimuli in the task. Individual hippocampal cells encoded visual stimuli only on specific types of trials in which retention of either, the Sample image, or the spatial position of the Sample image indicated at the beginning of the trial, was required. Consistent with such encoding, it was shown that patterned microstimulation applied during Sample image presentation facilitated selection of either Sample image spatial locations or types of images, during the Match phase of the task. These findings support the existence of specific codes for spatial and numeric object representations in primate hippocampus which can be applied on differentially signaled trials. Moreover, the transformational properties of hippocampal microcircuitry, together with the patterned microstimulation are supporting the practical importance of this approach for cognitive enhancement and rehabilitation, needed for memory neuroprosthetics.

No MeSH data available.


Related in: MedlinePlus

Hippocampal subfields CA1-CA3 firing in response to numeric categorization. Detection of numerosity features by numeric category selective hippocampal neurons. (A) Peri-event histogram arrays for six cells from CA1 that illustrate the selective numeric categorization of screen images. Thus, each row shows the firing response of one cell to the presentation of 2–7, images (in the Match phase) with the highest firing rate shaded in gray. Numeric categorization is illustrated by a color code so that red, orange, green, blue, dark blue and violet correspond to respectively 2, 3, 4, 5, 6, and 7 images on the screen. (B) The normalized activity for the cells in CA1 (A) and CA3 is shown for their selective category preference to the number of images. Note that both tuning plots to number categories (to CA1 and to CA3 in Figure 3S) show a distributed code. (C) The average firing activity across all selective cells in CA1 and CA3 with preferred numeric categories. Neurons in both subfields show significant firing preference for a given number of images. (D) Normalized average numeric tuning function across all preferred numeric categories and selective CA1 and CA3 neurons for the Match phase of the task. (E) Distributions of CA1 (red) and CA3 (blue) neurons with preferred numeric features in recorded during the Match phase of the DMS task. Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
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Figure 4: Hippocampal subfields CA1-CA3 firing in response to numeric categorization. Detection of numerosity features by numeric category selective hippocampal neurons. (A) Peri-event histogram arrays for six cells from CA1 that illustrate the selective numeric categorization of screen images. Thus, each row shows the firing response of one cell to the presentation of 2–7, images (in the Match phase) with the highest firing rate shaded in gray. Numeric categorization is illustrated by a color code so that red, orange, green, blue, dark blue and violet correspond to respectively 2, 3, 4, 5, 6, and 7 images on the screen. (B) The normalized activity for the cells in CA1 (A) and CA3 is shown for their selective category preference to the number of images. Note that both tuning plots to number categories (to CA1 and to CA3 in Figure 3S) show a distributed code. (C) The average firing activity across all selective cells in CA1 and CA3 with preferred numeric categories. Neurons in both subfields show significant firing preference for a given number of images. (D) Normalized average numeric tuning function across all preferred numeric categories and selective CA1 and CA3 neurons for the Match phase of the task. (E) Distributions of CA1 (red) and CA3 (blue) neurons with preferred numeric features in recorded during the Match phase of the DMS task. Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.

Mentions: Figure 4A shows peri-event histograms of individual cells recorded in CA1, in which each row represents a distinct cell and each column represents the firing of different cells, when presented the same number of images, from 2 to 7). For each of these cells (CA1, n = 6) and (CA3, n = 6) the firing pattern was compared across the number of images in the Match phase (Figure 3S). Each cell shows peak activity for a particular number of images and a systematic drop-off of activity as the number varied from that preferred value (Hauser et al., 1996; Nieder, 2005). Figure 4B is shows “numeric tuning” of the preferred normalized activity (Piazza et al., 2004) of the same neurons from CA1 (top) and CA3 (bottom). To rule out the fact that firing could represent a particular screen shape or configuration other than the number of images, Figure 4S shows 2 hippocampal cells that fire preferentially to four images but have a different spatial tuning on the Match phase screen.


Distributed encoding of spatial and object categories in primate hippocampal microcircuits.

Opris I, Santos LM, Gerhardt GA, Song D, Berger TW, Hampson RE, Deadwyler SA - Front Neurosci (2015)

Hippocampal subfields CA1-CA3 firing in response to numeric categorization. Detection of numerosity features by numeric category selective hippocampal neurons. (A) Peri-event histogram arrays for six cells from CA1 that illustrate the selective numeric categorization of screen images. Thus, each row shows the firing response of one cell to the presentation of 2–7, images (in the Match phase) with the highest firing rate shaded in gray. Numeric categorization is illustrated by a color code so that red, orange, green, blue, dark blue and violet correspond to respectively 2, 3, 4, 5, 6, and 7 images on the screen. (B) The normalized activity for the cells in CA1 (A) and CA3 is shown for their selective category preference to the number of images. Note that both tuning plots to number categories (to CA1 and to CA3 in Figure 3S) show a distributed code. (C) The average firing activity across all selective cells in CA1 and CA3 with preferred numeric categories. Neurons in both subfields show significant firing preference for a given number of images. (D) Normalized average numeric tuning function across all preferred numeric categories and selective CA1 and CA3 neurons for the Match phase of the task. (E) Distributions of CA1 (red) and CA3 (blue) neurons with preferred numeric features in recorded during the Match phase of the DMS task. Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
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Figure 4: Hippocampal subfields CA1-CA3 firing in response to numeric categorization. Detection of numerosity features by numeric category selective hippocampal neurons. (A) Peri-event histogram arrays for six cells from CA1 that illustrate the selective numeric categorization of screen images. Thus, each row shows the firing response of one cell to the presentation of 2–7, images (in the Match phase) with the highest firing rate shaded in gray. Numeric categorization is illustrated by a color code so that red, orange, green, blue, dark blue and violet correspond to respectively 2, 3, 4, 5, 6, and 7 images on the screen. (B) The normalized activity for the cells in CA1 (A) and CA3 is shown for their selective category preference to the number of images. Note that both tuning plots to number categories (to CA1 and to CA3 in Figure 3S) show a distributed code. (C) The average firing activity across all selective cells in CA1 and CA3 with preferred numeric categories. Neurons in both subfields show significant firing preference for a given number of images. (D) Normalized average numeric tuning function across all preferred numeric categories and selective CA1 and CA3 neurons for the Match phase of the task. (E) Distributions of CA1 (red) and CA3 (blue) neurons with preferred numeric features in recorded during the Match phase of the DMS task. Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
Mentions: Figure 4A shows peri-event histograms of individual cells recorded in CA1, in which each row represents a distinct cell and each column represents the firing of different cells, when presented the same number of images, from 2 to 7). For each of these cells (CA1, n = 6) and (CA3, n = 6) the firing pattern was compared across the number of images in the Match phase (Figure 3S). Each cell shows peak activity for a particular number of images and a systematic drop-off of activity as the number varied from that preferred value (Hauser et al., 1996; Nieder, 2005). Figure 4B is shows “numeric tuning” of the preferred normalized activity (Piazza et al., 2004) of the same neurons from CA1 (top) and CA3 (bottom). To rule out the fact that firing could represent a particular screen shape or configuration other than the number of images, Figure 4S shows 2 hippocampal cells that fire preferentially to four images but have a different spatial tuning on the Match phase screen.

Bottom Line: The primate hippocampus plays critical roles in the encoding, representation, categorization and retrieval of cognitive information.Four nonhuman primates were trained in a delayed-match-to-sample (DMS) task while multi-neuron activity was simultaneously recorded from the CA1 and CA3 hippocampal cell fields.The results show differential encoding of spatial location and categorization of images presented as relevant stimuli in the task.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Pharmacology, Wake Forest University School of Medicine Winston-Salem, NC, USA.

ABSTRACT
The primate hippocampus plays critical roles in the encoding, representation, categorization and retrieval of cognitive information. Such cognitive abilities may use the transformational input-output properties of hippocampal laminar microcircuitry to generate spatial representations and to categorize features of objects, images, and their numeric characteristics. Four nonhuman primates were trained in a delayed-match-to-sample (DMS) task while multi-neuron activity was simultaneously recorded from the CA1 and CA3 hippocampal cell fields. The results show differential encoding of spatial location and categorization of images presented as relevant stimuli in the task. Individual hippocampal cells encoded visual stimuli only on specific types of trials in which retention of either, the Sample image, or the spatial position of the Sample image indicated at the beginning of the trial, was required. Consistent with such encoding, it was shown that patterned microstimulation applied during Sample image presentation facilitated selection of either Sample image spatial locations or types of images, during the Match phase of the task. These findings support the existence of specific codes for spatial and numeric object representations in primate hippocampus which can be applied on differentially signaled trials. Moreover, the transformational properties of hippocampal microcircuitry, together with the patterned microstimulation are supporting the practical importance of this approach for cognitive enhancement and rehabilitation, needed for memory neuroprosthetics.

No MeSH data available.


Related in: MedlinePlus