Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information
- PMID: 11732710
- DOI: 10.1002/hipo.1073
Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information
Abstract
Processing of multimodal sensory information by the morphological subdivisions of the hippocampus and its input and output structures was investigated in unanesthetized rabbits by extracellular recording of neuronal activity. Analysis shows principal differences between CA3 neurons with uniform multimodal, mainly inhibitory, rapidly habituating sensory responses, and CA1-subicular neurons, substantial parts of which have phasic reactions and patterned on-responses, depending on the characteristics of the stimuli. These differences result from the organization of the afferent inputs to CA1 and CA3. Analysis of neuronal responses in sources of hippocampal inputs, their electrical stimulation, and chronic disconnection show the greater functional significance of the brain-stem reticular input for tonic responses characteristic of CA3. This input signal before entering the hippocampus is additionally preprocessed at the MS-DB relay, where it becomes more uniform and frequency-modulated in the range of theta-rhythm. It is shown that the new sensory stimuli produce inhibitory reset, after which synchronized theta-modulation is triggered. Other stimuli, appearing at the background of the ongoing theta, do not evoke any responses of the hippocampal neurons. Thus, theta-modulation can be regarded as a mechanism of attention, which prolongs response to a selected stimulus and simultaneously protects its processing against interference. The cortical input of the hippocampus introduces highly differentiated information analyzed at the highest levels of the neocortex through the intermediary of the entorhinal cortex and presubiculum. However, only CA1-subiculum receives this information directly; before its entrance into CA3, it is additionally preprocessed at the FD relay, where the secondary simplification of signals occurs. As a result, CA3 receives by its two inputs (MS-DB and FD) messages just about the presence and level of input signals in each of them, and performs relatively simple functions of determination of match/mismatch of their weights. For this comparator system, the presence of signal only in the reticulo-septal input is equivalent to quality of novelty. The cortical signal appears with some delay, after its analysis in the neocortex and shaping in the prehippocampal structures; besides, it is gradually increased due to LTP-like incremental changes in PP and mossy fiber synapses. The CA3 neurons with potentiated synapses of cortical input do not respond to sensory stimuli; that is, the increased efficacy of the cortical signals can be regarded as "familiarity" of a signal, terminating the reactive state of the CA3 neurons. The integrity of both inputs is necessary for gradual habituation of sensory responses in the hippocampus. The output signals of CA3 following in the precommissural fornix to the output relay-LS nucleus and to the brain-stem structures have strong regulatory influence on the level of brain activity (arousal), which is an important condition for processing and registration of information. The primary targets of this output signal are raphe nuclei, which suppress activity of the ascending excitatory RF. In the background state, activity of the CA3 neurons through the intermediary of raphe keeps RF under tonic inhibitory control. Inhibition of the majority of CA3 pyramidal neurons during a novel stimulus action decreases the volume of its output signal to raphe and releases RF from tonic inhibition (increase in level of activity of the forebrain, arousal). When the responses of CA3 neurons habituate, the initial high background activity is reinstated, as well as tonic suppression of RF. Analysis of the second output of CA3 (by Schaffer's collaterals to CA1) shows that activity in this pathway can block access of cortical signals from PP to CA1 neurons by action upon the local system of inhibitory neurons, or by shunting the propagation of signals in apical dendrites. Thus, CA3 can act as a filter controlling the information transmission by CA1; such transmission at any given moment is allowed only in those CA1 neurons which receive SC from CA3 neurons, responding to the sensory stimulus by suppression of their activity. Disconnection of the CA3 output fibers results in disappearance of habituation in all its target structures (raphe, RF, CA1). The output signal of CA1-subiculum follows by postcommissural fornix to the chain of structures of the main limbic circuit: mammillary bodies (medial nucleus), anterior thalamic nuclei (mainly antero-ventral nucleus), and cingulate limbic cortex (mainly posterior area). In each of these links, the signal is additionally processed. Habituation is nearly absent in these structures; instead, st
Similar articles
-
Pacemaker neurons of the forebrain medical septal area and theta rhythm of the hippocampus.Membr Cell Biol. 1998;11(6):715-25. Membr Cell Biol. 1998. PMID: 9718568 Review.
-
[Sensory reactions of hippocampal neurons in rabbit during functional suppression of theta rythm- controlling structures].Zh Vyssh Nerv Deiat Im I P Pavlova. 2001 Mar-Apr;51(2):228-35. Zh Vyssh Nerv Deiat Im I P Pavlova. 2001. PMID: 11548605 Russian.
-
[Effect of disconnecting cortical input on the activity of hippocampal neurons].Zh Vyssh Nerv Deiat Im I P Pavlova. 1976 Nov-Dec;26(6):1282-90. Zh Vyssh Nerv Deiat Im I P Pavlova. 1976. PMID: 1014902 Russian.
-
[The role of Schaffer's collaterals in the sensory responses of the neurons of hippocampal field CA1].Zh Vyssh Nerv Deiat Im I P Pavlova. 1975 Nov-Dec;25(6):1266-73. Zh Vyssh Nerv Deiat Im I P Pavlova. 1975. PMID: 1210777 Russian.
-
Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine.Hippocampus. 2001;11(5):551-68. doi: 10.1002/hipo.1071. Hippocampus. 2001. PMID: 11732708 Review.
Cited by
-
An Integrated Index: Engrams, Place Cells, and Hippocampal Memory.Neuron. 2020 Sep 9;107(5):805-820. doi: 10.1016/j.neuron.2020.07.011. Epub 2020 Aug 6. Neuron. 2020. PMID: 32763146 Free PMC article. Review.
-
Repetition suppression in the medial temporal lobe and midbrain is altered by event overlap.Hippocampus. 2016 Nov;26(11):1464-1477. doi: 10.1002/hipo.22622. Epub 2016 Aug 12. Hippocampus. 2016. PMID: 27479864 Free PMC article.
-
The error in total error reduction.Neurobiol Learn Mem. 2014 Feb;108:119-35. doi: 10.1016/j.nlm.2013.07.018. Epub 2013 Jul 25. Neurobiol Learn Mem. 2014. PMID: 23891930 Free PMC article. Review.
-
Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition.Nat Neurosci. 2012 Mar 25;15(5):769-75. doi: 10.1038/nn.3077. Nat Neurosci. 2012. PMID: 22446878 Free PMC article.
-
Memory influences on hippocampal and striatal neural codes: effects of a shift between task rules.Neurobiol Learn Mem. 2007 May;87(4):495-509. doi: 10.1016/j.nlm.2006.09.008. Epub 2007 Jan 19. Neurobiol Learn Mem. 2007. PMID: 17240173 Free PMC article.
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Research Materials
Miscellaneous