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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

Comparison of hippocampal firing to object image categorization. (A) Three individual cells from hippocampal subfields CA3 and CA1 illustrate preferred category firing for Sample images that display either flowers (green), animals (pink), or buildings (blue) as one of the image features. (B). Population mean firing from all cells in hippocampal subfields CA3 (right) and CA1 (left) in response to images that have features in preferred (in) vs. nonpreferred (out) categories. The number of cells with significant response to the same (animals, buildings and flowers) categories from CA3 is (animals: n = 39*/126, buildings: 37*/103, and flowers: 68*/81) and from CA1 is (animals: n = 25*/118, buildings: 41*/97; flowers: 42*/77). In each group are counted the cells with significant firing in the subgroup of cells satisfying inclusion criteria in the category. (C) Normalized category preferred tuning of the population of cells in CA3 (n = 23, 33, 54) and CA1 (n = 30, 54, 53). (D) Population histograms showing mean firing peaks in each category, as compared to other categories, for the same population of cells in Figure 4C. Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
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Figure 3: Comparison of hippocampal firing to object image categorization. (A) Three individual cells from hippocampal subfields CA3 and CA1 illustrate preferred category firing for Sample images that display either flowers (green), animals (pink), or buildings (blue) as one of the image features. (B). Population mean firing from all cells in hippocampal subfields CA3 (right) and CA1 (left) in response to images that have features in preferred (in) vs. nonpreferred (out) categories. The number of cells with significant response to the same (animals, buildings and flowers) categories from CA3 is (animals: n = 39*/126, buildings: 37*/103, and flowers: 68*/81) and from CA1 is (animals: n = 25*/118, buildings: 41*/97; flowers: 42*/77). In each group are counted the cells with significant firing in the subgroup of cells satisfying inclusion criteria in the category. (C) Normalized category preferred tuning of the population of cells in CA3 (n = 23, 33, 54) and CA1 (n = 30, 54, 53). (D) Population histograms showing mean firing peaks in each category, as compared to other categories, for the same population of cells in Figure 4C. Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.

Mentions: Cells in the hippocampus of NHPs are known to categorize objects and/or screen images according to the features and number of items seen (Hampson et al., 2004a, 2013; Kourtzi and Connor, 2011). Figure 3 shows the categorization of features that appear in randomly selected screen clip-art images used in the DMS task such as: flowers (green), animals (pink) and buildings (blue). The three hippocampal cells shown in Figure 3A respond with higher firing rates to only one image category and with lower firing when the other two illustrated images occurred in the Sample phase. This trend is consistent at the population level in which a subset of cells from both hippocampal subfields (Figure 3B) identified previously as having specificity for Sample phase firing (see above), also responded significantly (CA1, n = 165 cells; CA3, n = 143 cells; p < 0.001, ANOVA) to only one of three assessed image categories (flowers, animals or buildings) presented on different trials. Category specific activity for this subset of cells is shown in Figures 3C,D for normalized and peak firing rates, respectively.


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)

Comparison of hippocampal firing to object image categorization. (A) Three individual cells from hippocampal subfields CA3 and CA1 illustrate preferred category firing for Sample images that display either flowers (green), animals (pink), or buildings (blue) as one of the image features. (B). Population mean firing from all cells in hippocampal subfields CA3 (right) and CA1 (left) in response to images that have features in preferred (in) vs. nonpreferred (out) categories. The number of cells with significant response to the same (animals, buildings and flowers) categories from CA3 is (animals: n = 39*/126, buildings: 37*/103, and flowers: 68*/81) and from CA1 is (animals: n = 25*/118, buildings: 41*/97; flowers: 42*/77). In each group are counted the cells with significant firing in the subgroup of cells satisfying inclusion criteria in the category. (C) Normalized category preferred tuning of the population of cells in CA3 (n = 23, 33, 54) and CA1 (n = 30, 54, 53). (D) Population histograms showing mean firing peaks in each category, as compared to other categories, for the same population of cells in Figure 4C. Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
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Figure 3: Comparison of hippocampal firing to object image categorization. (A) Three individual cells from hippocampal subfields CA3 and CA1 illustrate preferred category firing for Sample images that display either flowers (green), animals (pink), or buildings (blue) as one of the image features. (B). Population mean firing from all cells in hippocampal subfields CA3 (right) and CA1 (left) in response to images that have features in preferred (in) vs. nonpreferred (out) categories. The number of cells with significant response to the same (animals, buildings and flowers) categories from CA3 is (animals: n = 39*/126, buildings: 37*/103, and flowers: 68*/81) and from CA1 is (animals: n = 25*/118, buildings: 41*/97; flowers: 42*/77). In each group are counted the cells with significant firing in the subgroup of cells satisfying inclusion criteria in the category. (C) Normalized category preferred tuning of the population of cells in CA3 (n = 23, 33, 54) and CA1 (n = 30, 54, 53). (D) Population histograms showing mean firing peaks in each category, as compared to other categories, for the same population of cells in Figure 4C. Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
Mentions: Cells in the hippocampus of NHPs are known to categorize objects and/or screen images according to the features and number of items seen (Hampson et al., 2004a, 2013; Kourtzi and Connor, 2011). Figure 3 shows the categorization of features that appear in randomly selected screen clip-art images used in the DMS task such as: flowers (green), animals (pink) and buildings (blue). The three hippocampal cells shown in Figure 3A respond with higher firing rates to only one image category and with lower firing when the other two illustrated images occurred in the Sample phase. This trend is consistent at the population level in which a subset of cells from both hippocampal subfields (Figure 3B) identified previously as having specificity for Sample phase firing (see above), also responded significantly (CA1, n = 165 cells; CA3, n = 143 cells; p < 0.001, ANOVA) to only one of three assessed image categories (flowers, animals or buildings) presented on different trials. Category specific activity for this subset of cells is shown in Figures 3C,D for normalized and peak firing rates, respectively.

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