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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

Microstimulation induced facilitation on preferred target location encoding and categorization. (A) Facilitated spatial tuning by delivery of MIMO stimulation. The facilitative effect of MIMO stimulation (Stim) vs. control (no-stim) trials shows both tuning and enhancement. (B) Performance difference between stimulation and control conditions across 10 sessions (s1–s10) illustrating the general trend of facilitated spatial tuning by MIMO Stim. (C) Comparison of the facilitation effect between MIMO stimulation and control conditions for Spatial tuning. Correct performance induced by MIMO stimulation (Stim) is compared with control (no-stim) conditions for cells that respond with spatial preferences (n = 20 sessions). (D) Comparison of the facilitation effect on categorization between MIMO stim (during the sample phase) and control (Nostim categorization). Altogether, the facilitated categorization and performance levels on MIMO Stim trials was significantly higher than the levels on no-stim trials (Facilitated vs. Control: p < 0.001; ANOVA). Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
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Figure 5: Microstimulation induced facilitation on preferred target location encoding and categorization. (A) Facilitated spatial tuning by delivery of MIMO stimulation. The facilitative effect of MIMO stimulation (Stim) vs. control (no-stim) trials shows both tuning and enhancement. (B) Performance difference between stimulation and control conditions across 10 sessions (s1–s10) illustrating the general trend of facilitated spatial tuning by MIMO Stim. (C) Comparison of the facilitation effect between MIMO stimulation and control conditions for Spatial tuning. Correct performance induced by MIMO stimulation (Stim) is compared with control (no-stim) conditions for cells that respond with spatial preferences (n = 20 sessions). (D) Comparison of the facilitation effect on categorization between MIMO stim (during the sample phase) and control (Nostim categorization). Altogether, the facilitated categorization and performance levels on MIMO Stim trials was significantly higher than the levels on no-stim trials (Facilitated vs. Control: p < 0.001; ANOVA). Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.

Mentions: To further test whether hippocampal firing encoded the position of the sample target, or the numerical representation of the match phase screen, we applied the patterned stimulation previously shown to facilitate performance in the DMS task (Hampson et al., 2013). The application of the multi-input multi-output (MIMO) nonlinear model allowed extraction of a configuration of electrical (bipolar) stimulation pulses (20 uA amplitude and 1 ms duration) delivered to the same CA1 subfield from which task-related firing was obtained (Figure 1D and Figure 5S). This is shown as a functional diagram in which neural firing in hippocampal subfield CA3 was recorded with a multi-electrode array (Hampson et al., 2004b; Santos et al., 2012) and fed into a nonlinear multi-input–multi-output (MIMO) math model. Alter processing input signals from CA3, a pattern of electrical pulses (from a multi-channel stimulator that mimicked the output signals of correlated firing of CA1 cells) was simultaneously delivered to CA1 electrode locations, in the Sample phase on correct trials (Hampson et al., 2013). The diagram of the MIMO model driving a multichannel stimulator with output to CA1 electrode locations is illustrated in Figure 5S. Figure 5A shows an example of MIMO stimulation with induced behavioral tuning to a preferred spatial location (0°) compared to the No-stim trials. Figure 5B shows the performance difference in 10 sessions illustrating the general trend of facilitated spatial tuning (Figure 5B).


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)

Microstimulation induced facilitation on preferred target location encoding and categorization. (A) Facilitated spatial tuning by delivery of MIMO stimulation. The facilitative effect of MIMO stimulation (Stim) vs. control (no-stim) trials shows both tuning and enhancement. (B) Performance difference between stimulation and control conditions across 10 sessions (s1–s10) illustrating the general trend of facilitated spatial tuning by MIMO Stim. (C) Comparison of the facilitation effect between MIMO stimulation and control conditions for Spatial tuning. Correct performance induced by MIMO stimulation (Stim) is compared with control (no-stim) conditions for cells that respond with spatial preferences (n = 20 sessions). (D) Comparison of the facilitation effect on categorization between MIMO stim (during the sample phase) and control (Nostim categorization). Altogether, the facilitated categorization and performance levels on MIMO Stim trials was significantly higher than the levels on no-stim trials (Facilitated vs. Control: p < 0.001; ANOVA). Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
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Figure 5: Microstimulation induced facilitation on preferred target location encoding and categorization. (A) Facilitated spatial tuning by delivery of MIMO stimulation. The facilitative effect of MIMO stimulation (Stim) vs. control (no-stim) trials shows both tuning and enhancement. (B) Performance difference between stimulation and control conditions across 10 sessions (s1–s10) illustrating the general trend of facilitated spatial tuning by MIMO Stim. (C) Comparison of the facilitation effect between MIMO stimulation and control conditions for Spatial tuning. Correct performance induced by MIMO stimulation (Stim) is compared with control (no-stim) conditions for cells that respond with spatial preferences (n = 20 sessions). (D) Comparison of the facilitation effect on categorization between MIMO stim (during the sample phase) and control (Nostim categorization). Altogether, the facilitated categorization and performance levels on MIMO Stim trials was significantly higher than the levels on no-stim trials (Facilitated vs. Control: p < 0.001; ANOVA). Error bars represent SEMs. Asterisks: *p < 0.01, **p < 0.001; ANOVA.
Mentions: To further test whether hippocampal firing encoded the position of the sample target, or the numerical representation of the match phase screen, we applied the patterned stimulation previously shown to facilitate performance in the DMS task (Hampson et al., 2013). The application of the multi-input multi-output (MIMO) nonlinear model allowed extraction of a configuration of electrical (bipolar) stimulation pulses (20 uA amplitude and 1 ms duration) delivered to the same CA1 subfield from which task-related firing was obtained (Figure 1D and Figure 5S). This is shown as a functional diagram in which neural firing in hippocampal subfield CA3 was recorded with a multi-electrode array (Hampson et al., 2004b; Santos et al., 2012) and fed into a nonlinear multi-input–multi-output (MIMO) math model. Alter processing input signals from CA3, a pattern of electrical pulses (from a multi-channel stimulator that mimicked the output signals of correlated firing of CA1 cells) was simultaneously delivered to CA1 electrode locations, in the Sample phase on correct trials (Hampson et al., 2013). The diagram of the MIMO model driving a multichannel stimulator with output to CA1 electrode locations is illustrated in Figure 5S. Figure 5A shows an example of MIMO stimulation with induced behavioral tuning to a preferred spatial location (0°) compared to the No-stim trials. Figure 5B shows the performance difference in 10 sessions illustrating the general trend of facilitated spatial tuning (Figure 5B).

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